Broadband 75–85 MHz radiofrequency fields disrupt magnetic compass orientation in night-migratory songbirds consistent with a flavin-based radical pair magnetoreceptor

The light-dependent magnetic compass sense of night-migratory songbirds can be disrupted by weak radiofrequency fields. This finding supports a quantum mechanical, radical-pair-based mechanism of magnetoreception as observed for isolated cryptochrome 4, a protein found in birds’ retinas. The exact identity of the magnetically sensitive radicals in cryptochrome is uncertain in vivo, but their formation seems to require a bound flavin adenine dinucleotide chromophore and a chain of four tryptophan residues within the protein. Resulting from the hyperfine interactions of nuclear spins with the unpaired electrons, the sensitivity of the radicals to radiofrequency magnetic fields depends strongly on the number of magnetic nuclei (hydrogen and nitrogen atoms) they contain. Quantum-chemical calculations suggested that electromagnetic noise in the frequency range 75–85 MHz could give information about the identity of the radicals involved. Here, we show that broadband 75–85 MHz radiofrequency fields prevent a night-migratory songbird from using its magnetic compass in behavioural experiments. These results indicate that at least one of the components of the radical pair involved in the sensory process of avian magnetoreception must contain a substantial number of strong hyperfine interactions as would be the case if a flavin–tryptophan radical pair were the magnetic sensor.

Recombination suppression and selection affect local ancestries in genomes of a migratory songbird

The patterns of genetic relatedness among individuals vary along the genome, representing fluctuation of local ancestry. The factors responsible for this variation have not been well studied in wild animals with ecological and behavioural relevance. Here, we characterise the genomic architecture of genetic relatedness in the Eurasian blackcap, an iconic songbird species in ecology and quantitative genetics of migratory behaviour. We identify 23 genomic regions with deviated local relatedness patterns, using a chromosome-level de novo assembly of the blackcap genome and whole-genome resequencing data of 179 individuals from nine populations with diverse migratory phenotypes. Five genomic regions show local relatedness patterns of polymorphic inversions, three of which are syntenic to polymorphic inversions known in the zebra finch. Phylogenetic analysis reveals these three polymorphic inversions evolved independently in the blackcap and zebra finch indicating convergence of polymorphic inversions. Population genetic analyses in these three inversions in the blackcap suggest balancing selection between two haplotypes in one locus and background selection in the other two loci. One genomic region with deviated local relatedness is under selection against gene flow by population-specific reduction in recombination rate. Other genomic islands including 11 pericentromeric regions consist of evolutionarily conserved and non-conserved recombination cold-spots under background selection. Two of these regions with non-conserved recombination suppression are known to be associated with population-specific migratory phenotypes, where local relatedness patterns support additional effects of population-specific selection. These results highlight how different forms of recombination suppression and selection jointly affect heterogeneous genomic landscape of local ancestries.

Impact of Light at Night Is Phase Dependent: A Study on Migratory Redheaded Bunting (Emberiza bruniceps)

Artificial light at night (LAN) alters the physiology and behavior of an organism; however, very little is known about phase-dependent effects of LAN, particularly, in night migratory songbirds. Therefore, in this study, we investigated whether the effects of LAN on daily activity and photoperiodic responses in the Palearctic Indian migratory songbird, redheaded buntings (Emberiza bruniceps), is dependent on the different phases of the night. Male buntings maintained under short photoperiod (8L:16D; L = 100 lux, D < 0.1 lux) in individual activity cages were exposed to LAN (2 lux) for 6 weeks either in 4 h bin given at the different phases of 16 h night (early, mid, or late at ZT 08–12, ZT 14–18, or ZT 20–24, respectively; n = 9 each group) or throughout 16 h night (all night light, n = 6, ZT 08–24, the time of lights ON was considered as Zeitgeber time 0, ZT 0). A group (n = 6) with no LAN served as control. The results showed that LAN at the different phases of night induced differential effects as shown by an intense activity during the night, altered melatonin and temperature rhythms, and showed an increase in body mass and body fattening, food intake, and gonadal size. Midnight light exposure has a greater impact on migration and reproduction linked phenotypes, which is similar to the ones that received light throughout the night. The highlights of this study are that (i) LAN impacts day-night activity behavior, (ii) its continuity with the day alters the perception of day length, (iii) birds showed differential sensitivity to LAN in a phase-dependent manner, (iv) the direction of placing LAN affects the daily responses, e.g., LAN in the early night was “accepted” as extended dusk but the late night was considered as early dawn, and (v) midnight LAN was most effective and induced similar responses as continuous LAN. Overall, LAN induces long day responses in short days and shows differential sensitivity of the different phases of the night toward the light. This information may be valuable in adopting a part-night lighting approach to help reduce the physiological burden, such as early migration and reproduction, of artificial lighting on the nocturnal migrants.

A magnet attached to the forehead disrupts magnetic compass orientation in a migratory songbird

For studies on magnetic compass orientation and navigation performance in small bird species, controlled experiments with orientation cages inside an electromagnetic coil system are the most prominent methodological paradigm. These are, however, not applicable when studying larger bird species and/or orientation behaviour during free flight. For this, researchers have followed a very different approach. By attaching small magnets to birds, they intended to deprive them of access to meaningful magnetic information. Unfortunately, results from studies using this approach appear rather inconsistent. As these are based on experiments with birds under free flight conditions, which usually do not allow exclusion of other potential orientation cues, an assessment of the overall efficacy of this approach is difficult to conduct. Here, we directly test the efficacy of small magnets for temporarily disrupting magnetic compass orientation in small migratory songbirds using orientation cages under controlled experimental conditions. We found that birds which have access to the Earth's magnetic field as their sole orientation cue show a general orientation towards their seasonally appropriate migratory direction. When carrying magnets on their forehead under these conditions, the same birds become disoriented. However, under changed conditions that allow birds access to other (i.e. celestial) orientation cues, any disruptive effect of the magnets they carry appears obscured. Our results provide clear evidence for the efficacy of the magnet approach for temporarily disrupting magnetic compass orientation in birds, but also reveal its limitations for application in experiments under free flight conditions.

The Influence of Different Light Wavelengths of Anthropogenic Light at Night on Nestling Development and the Timing of Post-fledge Movements in a Migratory Songbird

Many different aspects of an animal’s lifecycle such as its behavior, patterns of hormone activity, and internal clock time, can be affected by anthropogenic light at night (ALAN). Exposing an organism to ALAN during its early life could also have an impact on its development. Since photoperiod can trigger or schedule the migration timing of long-distance migratory birds, there is great potential for anthropogenic light to interact with photoperiod to affect timing. However, very little has been investigated regarding the impacts of ALAN on post-hatching development and migration timing. We investigated the impact of ALAN during nestling development in a long-distance migratory songbird to determine the potential impact on the timing of post-breeding movements in the wild. We experimentally manipulated the light by using programmable lighting, in the nest boxes of free-living nestlings of purple martin (Progne subis) in Manitoba, Canada. We exposed two groups of developing nestlings, from hatch to fledge date, to green or white LED lights (5 lux) during the night. We also included a control group that experienced natural, ambient light at night. We found that some adults abandoned their nests shortly after starting the experiment (4 of 15 nests in the white light treatment). For the nests that remained active, nestlings exposed to the white light treatment had higher weights (at day 20 or 22), later fledge dates (1.54 ± 0.37, 95% CI 0.80–2.28), and later colony departure date (2.84 ± 1.00, 95% CI 0.88–4.81), than young of the control group. Moreover, nestlings of both white and green light groups had longer nesting duration than nestlings of the control group. This study demonstrates the impact of ALAN on the development of post-breeding movement timing in nestlings of wild migratory birds. However, our results also indicate that green light may have less of an impact as compared to white light.

Early Breeding Conditions Followed by Reduced Breeding Success Despite Timely Arrival in an Alpine Migratory Songbird

Timing reproduction to coincide with optimal environmental conditions is key for many organisms living in seasonal habitats. Advance in the onset of spring is a particular challenge to migratory birds that must time their arrival without knowing the conditions on the breeding grounds. This is amplified at high elevations where resource availability, which is linked to snowmelt and vegetation development, shows much annual variation. With the aim of exploring the effects of variability in the onset of local resource availability on reproduction, we compared key life history events in an Alpine population of the Northern Wheatear (Oenanthe oenanthe) between years of contrasting timing of snowmelt. Based on remote sensed images, we identified 2020 as an exceptionally early snowmelt and green-up year compared to the preceding year and the long-term average. Individuals tracked with light-level geolocators arrived well before the snowmelt in 2020 and clutch initiation dates across the population were earlier in 2020 compared to 2019. However, observations from a citizen science database and nest monitoring data showed that the arrival-breeding interval was shorter in 2020, thus the advance in timing lagged behind the environmental conditions. While hatching success was similar in both years, fledging success was significantly reduced in 2020. A trophic mismatch in early 2020 could be a possible explanation for the reduced reproductive success, but alternative explanations cannot be excluded. Our results show that, despite the timely arrival at the breeding grounds and a contraction of the arrival-breeding interval, Wheatears were not able to advance breeding activities in synchrony with environmental conditions in 2020. Earlier reproductive seasons are expected to become more frequent in the future. We show that the negative effects of changing seasons in Alpine migratory birds might be similar to birds breeding at high latitudes, despite their shorter migratory distance.

Experimental manipulation of photoperiod influences migration timing in a wild, long-distance migratory songbird

Previous laboratory studies have demonstrated the role of photoperiod in cueing the migration timing of small land birds; however, how migration timing of young birds in wild environments develops in relation to these cues have rarely been investigated. Such investigations can make important contributions to our developing understanding of the phenotypic plasticity of migration timing to new conditions with climate change, where changes in the timing of nesting may expose juvenile birds to different photoperiods. We investigated the impact of manipulating photoperiod during nestling development in a long-distance migratory songbird on the timing of post-breeding movements in the wild. Using programmable lighting installed in the nest-boxes of purple martins ( Progne subis ), we exposed developing nestlings, from hatch to fledge date, to an extended photoperiod that matched the day length of the summer solstice in Manitoba, Canada. We found that birds with a simulated, earlier photoperiod had a longer nesting period and later fledge and autumn departure dates than control group birds. This study demonstrates the phenotypic plasticity of first-year birds to the ontogenetic effect of their hatch date in the formation of the timing of their first post-breeding movements. Further, we discuss how these results have implications for the potential use of assisted evolution approaches to alter migration timing to match new conditions with climate change.