Birds that migrate at night enter a state of sleepless mania and gorge on foods by day, behaviors mediated by their biological clocks
Imagine yourself on board a red-eye flight from Los Angeles to New York City, an eight-hour journey that begins at bedtime and ends at breakfast. Your plan to sleep during the flight is thwarted by sporadic turbulence and an uncomfortable seat. When you arrive at John F. Kennedy Airport, you feel dehydrated and grumpy, but you head straight to work for an important meeting. Fast food, caffeine and deadlines fuel your day’s full schedule. That night, you order Chinese takeout and eat it mindlessly in front of your laptop. You want nothing more than a warm shower and a long rest. Unfortunately, it’s time to head back to the airport for another red-eye flight.
Although such a schedule is far from ideal, it’s manageable every once in a while. But imagine for a moment that this is your daily routine—working by day and flying by night, for weeks on end. Imagine also that there are no drinks or food on the plane. Oh, and you are powering the flight by riding a stationary bicycle.
Migration requires dramatic seasonal changes in behavior and physiology, and these changes must be timed appropriately for successful migration. In late summer after nestlings fledge, birds begin to molt, replacing their ratty old feathers with sleek new ones. They also begin to gorge themselves. The flurry of activity around this time of year reflects this frantic, single-minded pursuit of food. The birds’ hyperphagia, or excessive eating, is accompanied by great changes in body weight and composition. The birds get very fat—and then they are gone, en route to their wintering grounds on a journey of several weeks. They spend the winter in warmer climates, where resources are sufficient for survival. In late winter, they grow new feathers again; afteward, there’s another weeks-long period of hyperphagia. When the days get longer and the temperature is just right, they’re off again, migrating to summer breeding grounds. Upon arrival, males establish territories. Pairs form. Nests are built. Soon, eggs are incubating, then hatching, and parents devote almost all of their energy to feeding chicks. If time permits, parents may mate again and have another clutch. Then, the cycle repeats (see Figure 2 below).
Migration likely brings to mind the familiar sight of geese flying overhead in their iconic V formation, honking stridently as they fly toward their faraway goal. But the migration of many birds is a rarely observed phenomenon. Most passerine birds, a group that includes songbirds and groups taxonomically related to them, migrate at night. Nocturnal migration has fascinated scientists and bird enthusiasts for a long time. What are the advantages for birds that migrate at night? How do they do it? When do they sleep? The answers to these questions are as yet incomplete. And often answers only beget more questions. Nevertheless, technological advances have facilitated a recent surge in migration research. A recurring theme of this work is that biological clocks are intimately involved in controlling nocturnal migration.
The Circadian Clock
Although nocturnal migration is common among passerine species, most of these birds are strictly diurnal during nonmigratory periods. As in all animals, an internal circadian clock synchronized to the daily light-dark cycle controls distinct behavioral patterns of activity and rest. This “clock” consists of a network of clock genes, which can be regulated by external stimuli, such as light. During migration, birds that are normally diurnal become active during both day and night. This change, which happens concurrently with the changing seasons, entails a major reorganization both of physiology and of behavior on a daily time scale. What happens to the circadian clock during nocturnal migration? Does the clock stop working? Does it alter signals sent to the body? Or do the brain and body react differently to clock signals during the migratory period?
The neurobiological details of nocturnal migratory behavior are not well understood, but research that one of us has done (Bartell) with the late Eberhard Gwinner from the Max Planck Institute for Ornithology demonstrates that the circadian clock controls Zugunruhe. When the light-dark cycle is replaced with constant dim light, effectively removing external time-of-day cues, a bird’s activity continues to show a daily rhythm of approximately 24 hours, indicating that an endogenous timing mechanism (the circadian clock) coordinates the distribution of activity across the day. Under nonmigratory conditions there is a single bout of activity during that 24-hour cycle, whereas during migratory conditions there are two distinct bouts of activity. Both the daytime behaviors and nighttime Zugunruhe activities are controlled by the internal clock. However, as the bird prepares for migration, the activity rhythms lengthen to last 27 to 28 hours. In essence, these birds have a slower-running internal clock. In most animals, a longer “internal day” increases the circadian drive to stay awake and be active for longer periods of time.
The circadian clock controlling nocturnal migratory activity is distinct from the one that controls daytime activity, at least in those species tested. The temporal patterns of the two bouts of activity interact with each other in complex ways. Under specific low-intensity lighting schedules, the daily activity becomes synchronized to the light cycle but the Zugunruhe activity does not. The result is that the nocturnal bout is delayed each day, a few minutes at a time, until Zugunruhe coincides with the timing of the daytime bout. When this happens, Zugunruhe is suppressed. Over time, the Zugunruhe clock drifts into the night again, and its expression is reestablished. Although the study conditions are artificial, the results demonstrate that a separate circadian clock, interacting with other clocks in the body, controls the timing of Zugunruhe. Seasonal changes in how these clocks interact determine whether migratory activity is expressed.
Work done by Gwinner and Leonida Fusani of the Università di Ferrara shows that during the migratory period, the amount of Zugunruhe activity depends on energy reserves and food availability, in addition to circadian and seasonal cues. This finding indicates that external stimuli influence clock-mediated behaviors. Migrants must occasionally rest and refuel for several days at stopover sites to maintain sufficient energy reserves to reach their destination. When lean birds encounter a food-rich stopover site, Zugunruhe is suppressed until birds recover their body weight. This ensures that the birds stay at the stopover site and take advantage of the resources there. In contrast, the intensity of Zugunruhe is not diminished in lean birds when food is unavailable at a stopover site, ensuring that the birds continue migrating until they reach more favorable refueling grounds.
Nocturnal migratory behavior is seasonal, occurring in the fall and again in the spring. Annual changes in day length provide a predictable, reliable, and highly accurate environmental cue for time of year. The changes in day length, or photoperiod, are more pronounced with increasing distance from the Equator. Accordingly, photoperiodic time measurement is common among a variety of temperate-zone organisms encompassing plants, insects and vertebrates. In the spring, longer days prompt birds to change from wintering activities to premigratory molt, fattening and spring migration, as well as gonadal development for reproduction. The photoperiodic control of seasonal reproduction has been studied much more extensively than the control of migration, but some of the principles are the same. Photoperiodic time measurement is made possible by the circadian clock. Light signals must occur at a particular time relative to the animal’s internal biological clock to stimulate seasonal migration and reproduction, so photo-inducibility is controlled by a circadian clock. In nature, only days of a certain length initiate photoperiodic responses such as migration or reproduction. In the laboratory, such responses can be induced when light shines on a bird at certain times of its internally mediated “night.” In birds, photoreceptors located deep in the brain are involved in perceiving photoperiod length. Even blind birds are able to determine photoperiod length. Under long-day conditions, photoreceptors trigger a cascade of hormonal and physiological changes. The mechanisms initiating fall migration are less understood, although short days induce migratory behavior in the fall.
In addition to photoperiod cues, some birds use an internal calendar, or a circannual clock. When these birds are kept under constant day length, they spontaneously exhibit Zugunruhe twice per year. Work by Gwinner has shown that circannual rhythms can persist in captivity for up to 12 annual cycles, the maximum life span of passerines in captivity. Circannual rhythmicity is distinct from behaviors cued by day length because it does not require external stimuli such as light. However, photoperiod shapes the internal rhythm so that it accurately reflects the annual cycle. Species vary in the robustness of circannual rhythms and their relative importance for seasonal timing. Endogenous circannual timing is more important for birds that overwinter near the Equator, where day length cues to instigate spring migration are absent, and for trans-equatorial migrants, who experience an inversion in the direction of photoperiod changes. For example, birds crossing from the Northern Hemisphere into the Southern Hemisphere in the fall transition from perceiving shortening days to perceiving lengthening days. Several studies demonstrate that circannual rhythms of Zugunruhe are more robust and precise in equatorial and transequatorial migrants, such as willow warblers (Phylloscopus trochilus), than in species that migrate shorter distances, including many North American migrants. However, this is not always the case, suggesting that circannual rhythms in Zugunruhe are not the only factor determining migratory programs. In the wild, the expression of migratory behavior is the result of the convergence of multiple factors including the internal circannual rhythm, genetic variation in migratory tendency, social cues, body condition and environmental stimuli such as photoperiod, temperature and food availability.
Navigation and Orientation
Recently published research led by Heiko Schmaljohann at the Institute of Avian Research of Vogelwarte Helgoland showed that the northern wheatear (Oenanthe oenanthe), a small nocturnal migrant, travels 9,300 miles from Alaska, across Siberia and central Asia, to wintering grounds in eastern Africa, a phenomenal distance fraught with challenges such as traversing the Arabian desert. How do the birds find their way? The recent development of lightweight geolocators has made tracking routes of small, migrating birds possible, revealing details such as course, distance, speed and number of rest stops. Geolocator technology is still very new, but migration scientists have already noted its enormous potential for studying navigation in migrating birds, including sensory mechanisms, spatiotemporal memory, evolutionary adaptation, learning and plasticity.
Before modern tracking devices, navigation and orientation were studied in the laboratory using enclosures known as Emlen funnels, named after the researchers who developed them in 1966. Birds were placed individually into funnel-shaped, paper enclosures. An ink pad formed the base of the enclosure, and a wire screen placed on top prevented escape. The pattern of footprints in the funnel indicated the direction of attempted flight. Experimental manipulation revealed stimuli used for orientation, for example, celestial projections onto the ceiling or magnetic fields. When birds express Zugunruhe in captivity, they orient themselves in a seasonally appropriate direction (for North American birds, south in autumn and north in spring). Emlen funnels are still used for studying the neurobiology of orientation and navigation, although recording techniques and data analyses have been modernized (see Figure 6). Behavioral experiments using Emlen funnels show that birds in the Northern Hemisphere know to fly south during the fall and north during the spring based on perception of seasonal changes in photoperiod, with the aid of their internal clock. As it turns out, migratory birds use a combination of navigational tools, including a genetically hard-wired directional sense, a magnetic compass, celestial cues and, in nocturnal migrants, patterns of light polarization at sunset.
The role of a circadian clock in regulating navigation is controversial. One school of thought among biologists and physicists alike is that the magnetoreceptor birds use to navigate is cryptochrome, a circadian clock protein, and that this magnetic compass may be calibrated each sunset to help birds fly in the proper direction. Other researchers, using a clock-shifting or “jet lag” experimental paradigm, have failed to find a direct role of circadian clocks in migration. Additional experimentation directly testing the role of circadian clocks in navigation is warranted.
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.
Sleep(lessness) and Mania
If birds are migrating during the night and foraging during the day, when do they sleep? It’s unlikely that migrating birds get a normal amount of sleep, given the demands of long stretches of flying night after night. Migration is physically and cognitively demanding. Birds exert tremendous amounts of energy, navigating in the dark for thousands of miles, encountering new territories daily in which they must find food and avoid predators. Even if they managed to grab a catnap here and there, how do they function on such a sleep deficit? Our hypothetical businessman, churning out energy via stationary bike to power his red-eye flight before taxing his brain at work, would be severely cognitively handicapped after two days on this schedule. Humans lose one IQ point per hour of sleep deficit. But migratory birds, apparently, have developed a way to maximize performance while minimizing sleep.
How much, when and how they sleep remains unknown, but we are beginning to fill in knowledge gaps. Many birds can engage in unihemispheric sleep, where one half of the brain and body sleeps while the other half remains awake, so the animal can engage in at least some physical activity during sleep. Perhaps migrating birds employ this tactic on the wing; perhaps birds are able to find time to nap during the day; or perhaps migrating birds are unique among animals in their ability to go without sleep. There is clear evidence for the last in white-crowned sparrows (Zonotrichia leucophrys). In a University of Wisconsin study measuring sleep in captive birds, migrating white-crowned sparrows spent 63 percent less time sleeping than their nonmigrating counterparts. Furthermore, the structure of sleep was altered in migrating birds, which entered the rapid-eye movement (REM) stage of sleep more quickly than nonmigrating birds (see Figure 9, below right). Reduced REM sleep latency has also been observed in sleep-deprived humans, although the implications for cognition and performance are unclear. The migrating birds in this study did not compensate for reduced nighttime sleep by increasing their sleep intensity, nor did they sleep during the day. Yet remarkably, their performance on a cognitive test that assessed learning ability did not decrease. Humans with a similar degree of sleep deprivation perform very poorly on similar tasks, and the same was true for sparrows in nonmigrating condition. When nonmigrating birds were prevented from sleeping, their performance declined as expected. Yet somehow the same birds, when migrating, are resistant to the effects of sleep restriction; indeed, both their cognitive function and physical performance are in top shape during the migratory period. How birds accomplish this feat remains a mystery, but when solved, efforts to improve cognitive function in people that are sleep-deprived as part of their profession, such as soldiers and pilots, could be refined.
In the study described above, the authors found no evidence of daytime sleep or of unihemispheric sleep in the migratory birds. However, daytime unihemispheric sleep and micronaps, short sleep episodes lasting around 12 seconds, were observed in migrating Swainson’s thrushes (Catharus ustulatus), according to studies by Verner Bingman’s group at Bowling Green State University. Short, light bouts of sleep may allow birds some sleep recuperation without a significant loss of foraging time or risk for exposure to predators. Does this sleeping behavior occur in the wild? More work is needed to understand why species differ in sleep strategies during the migratory period.
Migrating birds seem to defy the “rules” of physiology. They become obese yet are elite endurance athletes; they hardly sleep, yet their brains and bodies are in top shape. Return to the image of taking the red-eye, night after night, running on next to no sleep and quick snacks. Now imagine that, instead of dreading this exhausting nightmare, you approach the task with unbounded energy. You feel no need for sleep. It’s difficult to sit still. You don’t need that triple latte; in fact you already feel as if you’re running on 1,500 milligrams of caffeine, or something stronger. If your spouse insists that you stay home and get some sleep, rather than taking that red-eye flight, you find that you can’t lie still in bed. You’re up, pacing the room with an irresistible urge to go somewhere. Most people would find that such sensations stretched their circadian inclinations. It may be more than coincidence that these actions are also characteristic of mania in people.
The hallmarks of mania include hyperactivity, reduced sleep, changes in sleep architecture, increased metabolism, increased goal-oriented behavior and increased stress hormone levels. Mania in people often occurs on a seasonal basis. Because these hallmarks are also characteristic of avian nocturnal migration, birds may be a useful research model for the development and treatment of seasonally occurring mood disorders in humans, such as bipolar disorder.
The Next Leg
Migration, one of the most salient and captivating animal behaviors, continues to mystify us even as our knowledge of it grows. Migratory birds are giving us humans a run for our money. Superficially, their lives seem pretty attractive: They are immune to the maladaptive effects of body fat, they function well without sufficient sleep, they dwell in seasonally suitable locations. Although we still don’t fully understand how birds accomplish these feats, the answers are likely far from simple. At least one unifying principle can gratify our curiosity: Biological clocks are involved in virtually all aspects of migratory physiology and behavior. Perhaps people could learn a lesson from birds, and, rather than resisting our natural daily and seasonal rhythms, march to the beat of our own biological clocks.
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