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.

Localisation of cryptochrome 2 in the avian retina

Cryptochromes are photolyase-related blue-light receptors acting as core components of the mammalian circadian clock in the cell nuclei. One or more members of the cryptochrome protein family are also assumed to play a role in avian magnetoreception, but the primary sensory molecule in the retina of migratory birds that mediates light-dependent magnetic compass orientation has still not been identified. The mRNA of cryptochrome 2 (Cry2) has been reported to be located in the cell nuclei of the retina, but Cry2 localisation has not yet been demonstrated at the protein level. Here, we provide evidence that Cry2 protein is located in the photoreceptor inner segments, the outer nuclear layer, the inner nuclear layer and the ganglion cell layer in the retina of night-migratory European robins, homing pigeons and domestic chickens. At the subcellular level, we find Cry2 both in the cytoplasm and the nucleus of cells residing in these layers. This broad nucleic expression rather points to a role for avian Cry2 in the circadian clock and is consistent with a function as a transcription factor, analogous to mammalian Cry2, and speaks against an involvement in magnetoreception.

Magnetic Compass Orientation in a Palaearctic–Indian Night Migrant, the Red-Headed Bunting

Red-headed buntings (Emberiza bruniceps) perform long-distance migrations within their southerly overwintering grounds and breeding areas in the northern hemisphere. Long-distance migration demands essential orientation mechanisms. The earth’s magnetic field, celestial cues, and memorization of geographical cues en route provide birds with compass knowledge during migration. Birds were tested during spring migration for orientation under natural clear skies, simulated overcast skies at natural day length and temperature, simulated overcast at 22 °C and 38 °C temperatures, and in the deflected (−120°) magnetic field. Under clear skies, the red-headed buntings were oriented NNW (north–northwest); simulated overcast testing resulted in a northerly mean direction at local temperatures as well as at 22 °C and 38 °C. The buntings reacted strongly in favor of the rotated magnetic field under the simulated overcast sky, demonstrating the use of a magnetic compass for migrating in a specific direction.

A novel isoform of cryptochrome 4 (Cry4b) is expressed in the retina of a night-migratory songbird

The primary sensory molecule underlying light-dependent magnetic compass orientation in migratory birds has still not been identified. The cryptochromes are the only known class of vertebrate proteins which could mediate this mechanism in the avian retina. Cryptochrome 4 of the night-migratory songbird the European robin (Erithacus rubecula; erCry4) has several of the properties needed to be the primary magnetoreceptor in the avian eye. Here, we report on the identification of a novel isoform of erCry4, which we named erCry4b. Cry4b includes an additional exon of 29 amino acids compared to the previously described form of Cry4, now called Cry4a. When comparing the retinal circadian mRNA expression pattern of the already known isoform erCry4a and the novel erCry4b isoform, we find that erCry4a is stably expressed throughout day and night, whereas erCry4b shows a diurnal mRNA oscillation. The differential characteristics of the two erCry4 isoforms regarding their 24-h rhythmicity in mRNA expression leads us to suggest that they might have different functions. Based on the 24-h expression pattern, erCry4a remains the more likely cryptochrome to be involved in radical-pair-based magnetoreception, but at the present time, an involvement of erCry4b cannot be excluded.

Eyes are essential for magnetoreception in a mammal

Several groups of mammals use the Earth's magnetic field for orientation, but their magnetosensory organ remains unknown. The Ansell's mole-rat ( Fukomys anselli , Bathyergidae, Rodentia) is a microphthalmic subterranean rodent with innate magnetic orientation behaviour. Previous studies on this species proposed that its magnetoreceptors are located in the eye. To test this hypothesis, we assessed magnetic orientation in mole-rats after the surgical removal of their eyes compared to untreated controls. Initially, we demonstrate that this enucleation does not lead to changes in routine behaviours, including locomotion, feeding and socializing. We then studied magnetic compass orientation by employing a well-established nest-building assay under four magnetic field alignments. In line with previous studies, control animals exhibited a significant preference to build nests in magnetic southeast. By contrast, enucleated mole-rats built nests in random magnetic orientations, suggesting an impairment of their magnetic sense. The results provide robust support for the hypothesis that mole-rats perceive magnetic fields with their minute eyes, probably relying on magnetite-based receptors in the cornea.

Eyes are essential for magnetoreception in a mammal

Several groups of mammals use the Earth’s magnetic field for orientation, but their magnetosensory organ remains unknown. The Ansell’s mole-rat (Fukomys anselli) is a subterranean rodent with innate magnetic orientation behavior. Previous studies proposed that its magnetoreceptors are located in the eye. To test this hypothesis, we assessed magnetic orientation in enucleated mole-rats.Initially, we demonstrate that enucleation of mole-rats does not lead to changes in routine behaviors. We then studied magnetic compass orientation by employing a well-established nest building assay. To ensure that directional responses were based on magnetic parameters, we tested animals under four magnetic field alignments. In line with previous studies, control animals exhibited a significant preference to build nests in magnetic south-east. In contrast, enucleated mole-rats built nests in random magnetic orientations, suggesting an impairment of their magnetic sense. The results provide robust support for the hypothesis that mole-rats perceive magnetic fields with their minute eyes.

Electromagnetic 0.1–100 kHz noise does not disrupt orientation in a night-migrating songbird implying a spin coherence lifetime of less than 10 µs

According to the currently prevailing theory, the magnetic compass sense in night-migrating birds relies on a light-dependent radical-pair-based mechanism. It has been shown that radio waves at megahertz frequencies disrupt magnetic orientation in migratory birds, providing evidence for a quantum-mechanical origin of the magnetic compass. Still, many crucial properties, e.g. the lifetime of the proposed magnetically sensitive radical pair, remain unknown. The current study aims to estimate the spin coherence time of the radical pair, based on the behavioural responses of migratory birds to broadband electromagnetic fields covering the frequency band 0.1–100 kHz. A finding that the birds were unable to use their magnetic compass under these conditions would imply surprisingly long-lived (greater than 10 µs) spin coherence. However, we observed no effect of 0.1–100 kHz radiofrequency (RF) fields on the orientation of night-migratory Eurasian blackcaps ( Sylvia atricapilla ). This suggests that the lifetime of the spin coherence involved in magnetoreception is shorter than the period of the highest frequency RF fields used in this experiment (i.e. approx. 10 µs). This result, in combination with an earlier study showing that 20–450 kHz electromagnetic fields disrupt magnetic compass orientation, suggests that the spin coherence lifetime of the magnetically sensitive radical pair is in the range 2–10 µs.