avian migration

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46 American Scientist, Volume 101 © 2013 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected].

Imagine yourself on board a red-eye flight from Los Angeles to New York

City, an eight-hour journey that be-gins at bedtime and ends at breakfast. Your plan to sleep during the flight is thwarted by sporadic turbulence and an uncomfortable seat. When you ar-rive at John F. Kennedy Airport, you feel dehydrated and grumpy, but you head straight to work for an important meeting. Fast food, caffeine and dead-lines 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. Unfor-tunately, 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—work-ing by day and flying by night, for weeks on end. Imagine also that there

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

Paul Bartell and Ashli Moore

Paul Bartell is an assistant professor of avian biology at The Pennsylvania State University. His laborato-ry investigates the role of biological clocks in the reg-ulation of physiology and behavior. He received his Ph.D. from the University of Virginia. Ashli Moore is a researcher at Pennsylvania State University, where her research focuses on the ecology and evolu-tion of the vertebrate circadian clock. She received her Ph.D. in biology at the University of Virginia. Address for Bartell: 205 Henning Building, Animal Science, Pennsylvania State University, University Park, PA 16802. Email: [email protected]

2013 January–February 47www.americanscientist.org © 2013 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected].

are no drinks or food on the plane. Oh, and you are powering the flight by rid-ing a stationary bicycle.

Of course, this is absurd and impos-sible. Yet billions of birds perform an analogous routine twice a year as they migrate between summer breeding grounds and wintering grounds. Of the 700 or more bird species nesting in North America, more than 400 species migrate. Worldwide, migratory birds are declining faster than nonmigrants. Understanding the challenges that mi-gratory species face is an important conservation issue.

Migration requires dramatic season-al changes in behavior and physiol-ogy, 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 ac-companied 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 sur-vival. In late winter, they grow new feathers again; afteward, there’s an-other weeks-long period of hyperpha-gia. 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 hatch-ing, 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).

Migration likely brings to mind the familiar sight of geese flying overhead in their iconic V formation, honking stridently as they fly toward their far-away goal. But the migration of many birds is a rarely observed phenom-enon. Most passerine birds, a group that includes songbirds and groups taxonomically related to them, mi-grate at night. Nocturnal migration has fascinated scientists and bird en-thusiasts 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 ques-tions are as yet incomplete. And often answers only beget more questions. Nevertheless, technological advances have facilitated a recent surge in mi-gration research. A recurring theme of this work is that biological clocks are intimately involved in controlling nocturnal migration.

How do we know birds migrate at night? For a long time, people have ob-served that flocks of birds change loca-tion between evening and the following morning. Since around 1880, ornitholo-gists have used lunar observation—watching birds fly past the moon—to document nocturnal flights. A tally of nocturnal flight calls was published in 1899, although this technique did not flourish until the 1950s, when advances in sound recording made it more prac-tical. During the early days of radar technology in the 1940s, “phantom sig-nals” were discovered to be migrating birds. Radar has since become a widely used tool for monitoring bird migra-tions. Many of these classic methods are still used, with some modern im-provements. For example, with the aid of special microphones and automated sound detection software, ornithologists

Figure 1. Many passerine birds, including songbirds and their allies, migrate at night. Nocturnal migrators thus include a diverse array of birds, and a selection are shown above. From left to right, the species depicted are: blackcap (Sylvia atricapilla), European robin (Erithacus rubecula), chaffinch (Fringilla coelebs), painted bunting (Passerina ciris), white-crowned sparrow (Zonotrichia leucophrys), wood thrush (Hylocichla mustelina), American robin (Turdus migratorius), yellow warbler (Setophaga petechia), garden warbler (Sylvia borin) and black-headed bunting (Emberiza melanocephala).


recently reported in the Wilson Journal of Ornithology that pine siskins (Spinus pinus) undergo an irregular, nomadic type of nocturnal migration. Noctur-nal migration may be more widespread than previously thought.

Nocturnal migratory activity is also studied in the laboratory. In cap-tivity, night-migrating birds display

stereotypic migratory behaviors dur-ing the night known as Zugunruhe, meaning “migratory restlessness.” Birds exhibiting Zugunruhe flap their wings rapidly as if about to take off from the perch. The term was coined by German bird fanciers who caught and kept wild birds; they noticed that at night, during certain times of year,

their birds’ migratory proclivities re-sulted in damage to their feathers. This wing-whirring behavior can be clearly distinguished from captive birds’ day-time behaviors, such as hopping or feeding. Zugunruhe occurs during the dark period only. Because Zugunruhe behavior is maintained in the labora-tory, biologists have been able to study diverse subjects related to migration, including biological clocks, navigation, metabolism and sleep.

The Circadian ClockAlthough nocturnal migration is com-mon among passerine species, most of these birds are strictly diurnal dur-ing nonmigratory periods. As in all animals, an internal circadian clock syn-chronized 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. (For more details regarding clock genes, see the sidebar on page 53.) Dur-ing migration, birds that are normally diurnal become active during both day and night. This change, which hap-pens concurrently with the changing seasons, entails a major reorganization both of physiology and of behavior on

Figure 2. The migratory bird’s annual cycle (in this example, that of the white-throated sparrow, Zonotrichia albicollis) encompasses two bouts of migration, punctuated by repro-duction and overwintering. Following repro-duction, birds molt their feathers and bulk up on fattening foods to fuel their flight to warmer climes. In spring, as the days length-en, birds molt and bulk up again, returning to their summer breeding grounds, where they mate and raise their young.

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Figure 3. Screenshots from an infrared video taken during complete darkness show wing-whirring and migratory restlessness typical of a be-havior called Zugunruhe, which night-migrating birds display in captivity during the times of year that they would be migrating. (Photographs courtesy of Paul Bartell.)


a daily time scale. What happens to the circadian clock during nocturnal migration? Does the clock stop work-ing? 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 noc-turnal migratory behavior are not well understood, but research that one of us has done (Bartell) with the late Eb-erhard Gwinner from the Max Planck Institute for Ornithology demonstrates that the circadian clock controls Zu-gunruhe. When the light-dark cycle is replaced with constant dim light, ef-fectively removing external time-of-day cues, a bird’s activity continues to show a daily rhythm of approximately 24 hours, indicating that an endoge-nous timing mechanism (the circadian clock) coordinates the distribution of activity across the day. Under non-migratory conditions there is a single bout of activity during that 24-hour cycle, whereas during migratory con-ditions there are two distinct bouts of activity. Both the daytime behaviors and nighttime Zugunruhe activities are controlled by the internal clock. How-ever, as the bird prepares for migra-tion, 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 “inter-nal day” increases the circadian drive to stay awake and be active for longer periods of time.

The circadian clock controlling noc-turnal migratory activity is distinct from the one that controls daytime activ-ity, at least in those species tested. The temporal patterns of the two bouts of activity interact with each other in com-plex ways. Under specific low-intensity lighting schedules, the daily activity be-comes 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 dem-onstrate 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 Leoni-da Fusani of the Università di Ferrara shows that during the migratory pe-riod, the amount of Zugunruhe activ-ity depends on energy reserves and food availability, in addition to circa-dian 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 main-tain sufficient energy reserves to reach their destination. When lean birds en-counter a food-rich stopover site, Zu-gunruhe is suppressed until birds re-cover 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 Zu-gunruhe is not diminished in lean birds when food is unavailable at a stopover site, ensuring that the birds continue migrating until they reach more favor-able refueling grounds.

Nocturnal migratory behavior is seasonal, occurring in the fall and again in the spring. Annual changes in day length provide a predictable, reli-able, and highly accurate environmen-tal cue for time of year. The changes in day length, or photoperiod, are more pronounced with increasing distance from the Equator. Accordingly, pho-toperiodic time measurement is com-mon 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 premigra-tory molt, fattening and spring migra-tion, as well as gonadal development for reproduction. The photoperiodic control of seasonal reproduction has been studied much more extensive-ly 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 medi-ated “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 physiologi-cal changes. The mechanisms initiat-ing 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,

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Figure 4. Activity of a garden warbler (S. borin), indicated by black bars, in-creases as the simulated photoperiod decreases in the manner typical of mid-July through mid-August before fall migration. While daytime activity remains largely the same, dark pe-riod activity, or Zugunruhe, increases markedly. (Figure adapted from P. A. Bartell and E. Gwinner, Journal of Biological Rhythms 20: 538.)

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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 an-nual 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 in-ternal rhythm so that it accurately re-flects the annual cycle. Species vary in the robustness of circannual rhythms and their relative importance for sea-sonal timing. Endogenous circannual timing is more important for birds that overwinter near the Equator, where day length cues to instigate spring migra-tion are absent, and for trans-equatorial migrants, who experience an inver-sion in the direction of photoperiod changes. For example, birds crossing from the Northern Hemisphere into the Southern Hemisphere in the fall transi-tion from perceiving shortening days to perceiving lengthening days. Sev-eral studies demonstrate that circan-nual rhythms of Zugunruhe are more

robust and precise in equatorial and transequatorial migrants, such as wil-low warblers (Phylloscopus trochilus), than in species that migrate shorter dis-tances, including many North Ameri-can migrants. However, this is not always the case, suggesting that circ-annual 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 in-cluding the internal circannual rhythm, genetic variation in migratory tendency, social cues, body condition and envi-ronmental stimuli such as photoperiod, temperature and food availability.

Navigation and OrientationRecently published research led by Heiko Schmaljohann at the Institute of Avian Research of Vogelwarte Hel-goland 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 scien-tists 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 stud-ied 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 en-closure, and a wire screen placed on top prevented escape. The pattern of footprints in the funnel indicated the direction of attempted flight. Experi-mental manipulation revealed stimuli used for orientation, for example, ce-lestial projections onto the ceiling or magnetic fields. When birds express Zugunruhe in captivity, they orient themselves in a seasonally appropri-ate direction (for North American birds, south in autumn and north in

spring). Emlen funnels are still used for studying the neurobiology of ori-entation and navigation, although re-cording techniques and data analyses have been modernized (see Figure 6). Behavioral experiments using Emlen funnels show that birds in the North-ern 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 geneti-cally 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 regu-lating navigation is controversial. One school of thought among biologists and physicists alike is that the magne-toreceptor birds use to navigate is cryp-tochrome, a circadian clock protein, and that this magnetic compass may be calibrated each sunset to help birds fly in the proper direction. Other research-ers, 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, an-other typically day-active species, take red-eye flights because they offer cer-tain 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 di-urnal and nocturnal migration in all North American bird species to identi-fy factors associated with daily migra-tion. 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 en-ergetic costs due to decreased air tur-bulence. 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.

Figure 5. The development of lightweight geolocators, such as this one worn as a back-pack by a Swainson’s thrush (Catharus us-tulatus), is filling knowledge gaps about migration routes, times, and stopovers. (Pho-tograph by Kira Delmore, courtesy of the University of British Columbia.)


Energy, Metabolism and ClocksMigration 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 non-stop, 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. Neverthe-less, birds are hardly loafing. Aerobi-cally 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 exer-cise 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 inef-ficient, 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 spe-cies, a change in metabolic efficiency prompts fat accumulation, even with-out increased food intake. For the most part, however, seasonal changes in appetite and satiety lead to increased food intake, accounting for a signifi-cant amount of the body mass in many species. The hypothalamic region of the brain controls appetite and satiety,

and seasonal increases in neurotrans-mitters in the hypothalamus (for ex-ample, one called neuropeptide Y) are associated with seasonal hyperphagia in birds.

In mammals, a major signal for sa-tiety, 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

Figure 6. Emlen funnels have been used to study how migrating birds are able to deter-mine direction. In the original design, birds were placed on an inkpad so their footprints would be recorded along the paper-lined wall of the funnel (a). Modernized versions of the Emlen funnel are more quantitative, using mo-tion sensors that send data to a computer (b).

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Figure 7. Lean birds lacking fat are typical of the nonmigratory condition (left). Birds accumulate considerable amounts of subcutaneous fat in preparation for migration (right). (Photograph courtesy of Paul Bartell.)

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and lipid utilization in migratory birds. Strangely, the gene that encodes leptin is absent from the avian genome. How-ever, research from Christopher Gug-lielmo 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 re-ceptors. Adiponectin promotes glucose and fatty acid mobilization and metabo-lism, so levels of this molecule are usu-ally higher in lean animals. Like numer-ous other metabolic factors, adiponectin is rhythmically expressed in a circadian manner (see Figure 8). Work from our laboratory shows that when white-throated sparrows (Zonotrichia albicol-lis) 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 mi-gration distance: The longer the migra-tory 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 re-duction in digestive organ sizes, and bulking up flight muscles helps power the extra load. Still, the body condi-tion of a premigratory bird is in stark contrast to the human athlete prepar-ing 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 cardio-vascular disease. By human standards, premigratory birds are obese, diabetic and likely to drop dead of a heart at-tack at any moment. However, un-like 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 mobiliza-tion and oxidation that allow them to utilize fat at roughly 10 times the ca-pacity of mammals. During migration, these capabilities are further enhanced, allowing for a high degree of efficiency in fat utilization and storage. For ex-ample, 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 dur-ing refueling at stopover sites, evidence suggests that birds select food sources with higher fat content, particularly unsaturated fats that are used more ef-ficiently, 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 ac-quisition 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 con-structed of so-called clock genes and clock proteins, detailed in the sidebar on the opposite page.

The network of interactions be-tween the molecular clock and meta-bolic hormones is extremely complex. The links between lipid metabolism and the molecular clock are the subject of intense research because of their im-plications 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 remark-ably 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) exhibit-ing 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 circa-dian clock in the liver becomes stronger and more dominant as greater emphasis is placed on metabolism for flight as opposed to other behaviors or physi-ological processes. This study was con-ducted 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

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Figure 8. Under nonmigrating conditions, levels of the hormone adiponectin, which promotes glucose and fatty acid mobilization and metabolism, fluctuate rhythmically. When migrating, the rhythm is altered such that adiponectin levels peak during the night.


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 nu-trient 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 ef-fects, and instead focus on global changes in metabolism associated with migration. The study on blackcaps ex-hibiting Zugunruhe mentioned above suggests that during the day, the clock in the liver primes the bird’s body for more efficient nocturnal flight by in-ducing increases in PPARγ (see sidebar). 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, re-ferred to as migratory syndrome.

These experiments underscore the complex relationship between the cir-cadian clock, fat metabolism and mi-gration. We don’t yet fully understand this system or how it changes during migration. Clearly, an internal circan-nual clock controls seasonal changes in both fatty acid metabolism and the liver clock, and these changes are as-sociated with migratory state. Further work is needed to unravel the causal relationships.

Sleep(lessness) and ManiaIf 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, giv-en the demands of long stretches of fly-ing night after night. Migration is phys-ically 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, churn-ing out energy via stationary bike to power his red-eye flight before taxing his brain at work, would be severely

There are four main players in the vertebrate circadian clock, which are known as CLOCK, BMAL, Period (Per) and Cryptochrome (Cry). The core cir-cadian clock loop is a 24-hour cycle of alternating levels of these four com-ponents (below, at right). The process of copying DNA to RNA to make proteins is called transcription. Many genes are preceded by a segment of DNA, called a promoter, that initiates transcription of the gene in the pres-ence or absence of a certain molecule. CLOCK and BMAL proteins work as a pair to activate transcription of Per and Cry genes through Enhancer-box (E-box) elements found in the promoter regions of Per and Cry genes. When levels of Per and Cry protein accumu-late, they bind to the CLOCK/BMAL complex and inhibit their ability to activate gene transcription, includ-ing genes Per and Cry. This shutdown causes levels of Per and Cry protein to decline, because these proteins regu-larly degrade in the cell. Once Per and Cry protein levels decline to a specif-ic point, CLOCK/BMAL once again activate transcription of Per and Cry genes, and the cycle begins again. This molecular transcription-translation feedback loop occurs in cells all over the body, and groups of cells are coor-dinated in certain organs to perform special clock functions. In the brain, for example, a “master clock” coordi-nates timing in “peripheral clocks,” such as the clock in the liver that con-trols the timing of nutrient metabolism and energy homeostasis.

In addition to Per and Cry, the CLOCK/BMAL complex also pro-motes the rhythmic transcription of many other genes, in particular those that also contain E-box elements in their promoter regions. One of these is peroxisome proliferator activating receptor (PPAR), a protein involved in energy homeostasis and metabolism. Different forms of PPAR (pronounced “pee-par”) have distinct functions. PPARα is found primarily in the liver and promotes lip-id metabolism by activating the tran-scription of many genes involved in fat breakdown. PPARγ, on the other hand, promotes fat production and storage. Because eating is a circadian behavior in many animals, these compounds

may be regulated in a circadian man-ner. The storage of nutrients and their breakdown for energy are opposing processes, so their temporal separation would avoid physiological conflict.

In addition to the circadian control of PPAR expression, PPAR is linked to the liver clock in other ways. Per pro-tein inhibits fat production by regulat-ing PPARγ (see red line from Per to PPAR below). Since Per cycles rhythmically, so would its regulation of PPARγ’s tran-scriptional activity, effectively making PPARγ function rhythmic. PPARs also regulate the circadian clock by induc-ing the expression of the clock protein BMAL. Thus, PPAR controls and is controlled by the molecular clock.

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cognitively handicapped after two days on this schedule. Humans lose one IQ point per hour of sleep deficit. But mi-gratory birds, apparently, have devel-oped a way to maximize performance while minimizing sleep.

How much, when and how they sleep remains unknown, but we are be-ginning 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 tac-tic on the wing; perhaps birds are able to find time to nap during the day; or per-haps 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. Fur-thermore, the structure of sleep was al-tered in migrating birds, which entered the rapid-eye movement (REM) stage of sleep more quickly than nonmigrating birds (see Figure 9). Reduced REM sleep latency has also been observed in sleep-deprived humans, although the impli-cations 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 non-migrating birds were prevented from sleeping, their performance declined as expected. Yet somehow the same birds, when migrating, are resistant to the ef-fects of sleep restriction; indeed, both their cognitive function and physical performance are in top shape during the migratory period. How birds accom-plish this feat remains a mystery, but when solved, efforts to improve cogni-tive 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 migrat-ing Swainson’s thrushes (Catharus us-tulatus), according to studies by Verner Bingman’s group at Bowling Green State University. Short, light bouts of sleep may allow birds some sleep recupera-tion without a significant loss of forag-ing time or risk for exposure to preda-tors. 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, in-stead of dreading this exhausting night-mare, you approach the task with un-bounded 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 mil-ligrams of caffeine, or something stron-ger. 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, pac-ing 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 hy-peractivity, reduced sleep, changes in sleep architecture, increased metabo-lism, increased goal-oriented behavior and increased stress hormone levels. Mania in people often occurs on a sea-sonal basis. Because these hallmarks are also characteristic of avian noctur-nal migration, birds may be a useful research model for the development

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Figure 9. In the laboratory, migrating white-crowned sparrows (Z. leucophrys) spent significantly less time sleeping than nonmigrating spar-rows. The structure of sleep in the two groups of birds was also markedly different; migrating birds entered the rapid-eye movement (REM) stage of sleep (dark purple) more quickly than nonmigrating birds do. (Figure adapted from N. C. Rattenborg, et al. PLOS Biology. 2:e212.)


and treatment of seasonally occurring mood disorders in humans, such as bipolar disorder.

The Next LegMigration, 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. Superfi-cially, 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. Al-though 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 in-volved in virtually all aspects of migra-tory 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.

BibliographyBairlein, F. 2002. How to get fat: Nutritional

mechanisms of seasonal fat accumulation in migratory songbirds. Naturwissenschaften 89:1–10.

Bairlein, F., D. R. Norris, R. Nagel, M. Bulte, C. C. Voigt, J. W. Fox, D. J. T. Hussell and H. Schmaljohann. 2012. Cross-hemisphere migration of a 25 g songbird. Biology Letters 8:505–507.

Bartell, P. A., and E. Gwinner. 2005. A separate circadian oscillator controls nocturnal migra-tory restlessness in the songbird Sylvia borin. Journal of Biological Rhythms 20:538–549.

Beauchamp, G. 2011. Why migrate during the day: A comparative analysis of North American birds. Journal of Evolutionary Biol-ogy 24:1969–1974.

Charoensuksai, P., and W. Xu. 2010. PPARs in rhythmic metabolic regulation and implica-tions in health and disease. PPAR Research 2010:1–9.

Emlen, S. T., and J. T. Emlen. 1966. A technique for recording migratory orientation of cap-tive birds. Auk 83:361–367.

Farner, D. S. 1964. The photoperiodic control of reproductive cycles in birds. American Scientist 52:137–156.

Fuchs, T., D. Maury, F. R. Moore and V. P. Bing-man. 2009. Daytime micro-naps in a noc-turnal migrant: An EEG analysis. Biology Letters 5:77–80.

Fusani, L., M. Cardinale, C. Carere and W. Goyman. 2009. Stopover decision during migration: Physiological conditions predict nocturnal restlessness in wild passerines. Biology Letters 5:302–309.

Guglielmo, C. G. 2010. Move that fatty acid: Fuel selection and transport in migratory birds and bats. Integrative and Comparative Biology 50:336–345.

Gwinner, E. 1996. Circadian and circannual

programmes in avian migration. Journal of Experimental Biology 199:39–48.

Gwinner, E. 2003. Circannual rhythms in birds. Current Opinion in Neurobiology 13:770–778.

Helm, B. 2006. Zugunruhe of migratory and non-migratory birds in a circannual con-text. Journal of Avian Biology 37:533–540.

McWilliams, S. R., C. Guglielmo, B. Pierce and M. Klaassen. 2004. Flying, fasting, and feed-ing in birds during migration: A nutritional and physiological ecology perspective. Jour-nal of Avian Biology 35:377–393.

Rattenborg, N. C., B. H. Mandt, W. H. Ober-meyer, P. J. Winsauer, R. Huber, M. Wikelski and R. M. Benca. 2004. Migratory sleepless-ness in the white-crowned sparrow (Zono-trichia leucophrys gambelii). PLoS Biology 2:924–936.

Watson, M. L., J. V. Wells and R. W. Bavis. 2011. First detection of night flight calls by pine siskins. Wilson Journal of Ornithology 123:161–164.

Weber, J. 2009. Commentary: The physiology of long-distance migration: Extending the limits of endurance metabolism. Journal of Experimental Biology 212:593–597.

For relevant Web links, consult this issue of American Scientist Online:

http://www.americanscientist.org/ issues/id.100/past.aspx

Flying Cars

hover above slow trucks—in the name of Pegasus they wing past

stucco houses, commercial strips, miniature golf,and the pale sand of the public beach.

Like poets, the designers test roll, pitch, and yaw. They practice gliding,

learn to wrap the extraordinary vertical in the everyday horizontal.

Developer Harry Culver plans a skyburb with an airplane in every garage.

The flying car ascends, amazes, yet, like a complex figure of speech,

the roadable airplane must land, fold its wings, drive on.

A flock of names whispers lift:Sky Flivver, Arrowplane, Autoplane, Airphibian.

—Dolores Hayden

avian migration

Documents

pennsylvania state university

university park

university of virginia

research triangle park

avian migration

biological clockspaul

ashli moorepaul bartell

state of sleepless mania