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
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.
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