Flexibility and Control of Circadian Activity, Migratory Restlessness and Fueling in Two Songbird Migrants

Susanne Åkesson,Mihaela Ilieva,Giuseppe Bianco

doi:10.3389/fevo.2021.666176

Abstract

Juvenile songbirds rely on an endogenous program, encoding direction, distance, fueling, and timing of migration. Migratory distance is species-specific, expressed as a period of migratory restlessness, for which the length is correlated with distance, while fueling is modified to meet anticipated flight distances controlled by geomagnetic cues and amount of day-light available for foraging. How daylength affect onset and level of migratory activity and fueling decisions in wild birds have so far received limited attention. Here we study how photoperiod controls onset, level and extent of autumn migratory activity and fueling in juvenile diurnally migrating dunnocks, and nocturnally migrating European robins by experimentally increasing daylength. For both species, we kept a control group indoors at the location of capture in southern Sweden exposed to the natural photoperiod, and an experimental group with increased and advanced photoperiod by 2 h in the morning. Dunnocks initiated migratory activity at sunrise (or artificial sunrise) in both groups, demonstrating a highly responsive and flexible component for the onset of migration triggered by light. Experimental robins anticipated the end of nocturnal migratory activity predicting the earlier sunrise immediately after the time-shift and expressed this behavior already under darkness, supporting a fast-resetting mechanism to the new diel period. Timing of end of morning activity was not affected by the earlier sunrise in both species, suggesting a fixed endogenous control that persisted throughout the 13-day study period. Experimental dunnocks expressed higher overall activity and lower fuel loads than controls, while robins did not change their overall activity and fuel load in response to the shifted and increased photoperiod. These results reveal important adaptations for circadian timekeeping including both a flexible onset open to fast modifications and a more rigid end, with differential effects by the treatment on migratory activity and fueling in the two species.

Highlights

Migratory naïve songbirds rely on an endogenous migration program guiding them from the sites where they are born to their wintering areas (Gwinner, 1975, 1996; Berthold, 1996)
Additional phenotypical adaptations are needed to enable successful long-distance migrations, including morphology, physiology, and behavior (Åkesson and Hedenström, 2007). Several of those adaptations are tightly connected to the endogenous migration program (Gwinner, 1975, 1996; Åkesson et al, 2017) and the ability to navigate (e.g., Emlen, 1975; Able, 1980; Åkesson et al, 2014), while others are related to disposition of time between fueling and flight (Hedenström and Alerstam, 1997). Both timing and length of the autumn migratory restlessness period have been shown to be correlated with migratory distance in songbirds (Berthold, 1973) and contribute to the individual variation and flexibility in migratory traits observed in birds (Åkesson and Helm, 2020)
We found that the experimental juvenile dunnocks responded to our earlier onset of sunrise experiment, by increasing the period of diurnal migratory activity, in contrast to what has been proposed for diurnal animals (Daan, 1976)

Summary

Introduction

Migratory naïve songbirds rely on an endogenous migration program guiding them from the sites where they are born to their wintering areas (Gwinner, 1975, 1996; Berthold, 1996). Additional phenotypical adaptations are needed to enable successful long-distance migrations, including morphology, physiology, and behavior (Åkesson and Hedenström, 2007) Several of those adaptations are tightly connected to the endogenous migration program (Gwinner, 1975, 1996; Åkesson et al, 2017) and the ability to navigate (e.g., Emlen, 1975; Able, 1980; Åkesson et al, 2014), while others are related to disposition of time between fueling and flight (Hedenström and Alerstam, 1997). The complex circadian pace-making system in birds include three main components (i.e., encephalic photoreceptors, pineal gland, and retina), shown to enable coordination of time over annual and circadian cycles (Gwinner and Brandstätter, 2001)

Methods

Results

Conclusion