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In European Robins, Erithacus rubecula, the magnetic compass is lateralized in favor of the right eye/left hemisphere of the brain. This lateralization develops during the first winter and initially shows a great plasticity. During the first spring migration, it can be temporarily removed by covering the right eye. In the present paper, we used the migratory orientation of robins to analyze the circumstances under which the lateralization can be undone. Already a period of 1½ h being monocularly left-eyed before tests began proved sufficient to restore the ability to use the left eye for orientation, but this effect was rather short-lived, as lateralization recurred again within the next 1½ h. Interpretable magnetic information mediated by the left eye was necessary for removing the lateralization. In addition, monocularly, the left eye seeing robins could adjust to magnetic intensities outside the normal functional window, but this ability was not transferred to the “right-eye system”. Our results make it clear that asymmetry of magnetic compass perception is amenable to short-term changes, depending on lateralized stimulation. This could mean that the left hemispheric dominance for the analysis of magnetic compass information depends on lateralized interhemispheric interactions that in young birds can swiftly be altered by environmental effects.
The magnetic compass of a migratory bird, the European robin (Erithacus rubecula), was shown to be lateralized in favour of the right eye/left brain hemisphere. However, this seems to be a property of the avian magnetic compass that is not present from the beginning, but develops only as the birds grow older. During first migration in autumn, juvenile robins can orient by their magnetic compass with their right as well as with their left eye. In the following spring, however, the magnetic compass is already lateralized, but this lateralization is still flexible: it could be removed by covering the right eye for 6 h. During the following autumn migration, the lateralization becomes more strongly fixed, with a 6 h occlusion of the right eye no longer having an effect. This change from a bilateral to a lateralized magnetic compass appears to be a maturation process, the first such case known so far in birds. Because both eyes mediate identical information about the geomagnetic field, brain asymmetry for the magnetic compass could increase efficiency by setting the other hemisphere free for other processes.
The GPS recorder consists of a GPS receiver board, a logging facility, an antenna, a power supply, a DC-DC converter and a casing. Currently, it has a weight of 33 g. The recorder works reliably with a sampling rate of 1/s and with an operation time of about 3 h, providing time-indexed data on geographic positions and ground speed. The data are downloaded when the animal is recaptured. Prototypes were tested on homing pigeons. The records of complete flight paths with surprising details illustrate the potential of this new method that can be used on a variety of medium-sized and large vertebrates.
This paper describes a first version of the GPS flight recorder for homing pigeons. The GPS recorder consists of a hybrid GPS board, a patch antenna 19*19 mm, a 3 V Lithium battery as power supply, a DCDC converter, a logging facility and an additional microprocessor. It has a weight of 33g. Prototypes were tested and worked reliably with a sampling rate of 1/sec and with an operation time of about 3 h. In first tests on homing pigeons 9 flight paths were recorded, showing details like loops flown immediately after the release, complete routes over 30 km including detours, rest periods and speed.
Flight paths of homing pigeons were measured with a newly developed recorder based on GPS. The device consists of a GPS receiver board, a logging facility, an antenna, a power supply, a DCDC converter and a casing. It has a weight of 33g and works reliably with a sampling rate of 1/s with an operation time of about 3 h, providing timeindexed data on geographic positions, ground speed and altitude. The data are downloaded when the bird is recaptured. The devices are fixed to the birds with a harness. The measured complete flight paths show many details: e.g. initial loops flown immediately after release and large detours flown by some pigeons. We are here presenting 3 examples of flight paths from a release site 17.3 km Northeast of the home loft in Frankfurt. Mean speed in flight, duration of breaks and length of the flight path were calculated. The pigeons chose different routes and have different individual tendencies to fly loops over the village close to the release site.
Oscillating magnetic field disrupts magnetic orientation in Zebra finches, Taeniopygia guttata
(2009)
Background Zebra finches can be trained to use the geomagnetic field as a directional cue for short distance orientation. The physical mechanisms underlying the primary processes of magnetoreception are, however, largely unknown. Two hypotheses of how birds perceive magnetic information are mainly discussed, one dealing with modulation of radical pair processes in retinal structures, the other assuming that iron deposits in the upper beak of the birds are involved. Oscillating magnetic fields in the MHz range disturb radical pair mechanisms but do not affect magnetic particles. Thus, application of such oscillating fields in behavioral experiments can be used as a diagnostic tool to decide between the two alternatives. Methods In a setup that eliminates all directional cues except the geomagnetic field zebra finches were trained to search for food in the magnetic north/south axis. The birds were then tested for orientation performance in two magnetic conditions. In condition 1 the horizontal component of the geomagnetic field was shifted by 90 degrees using a helmholtz coil. In condition 2 a high frequently oscillating field (1.156 MHz) was applied in addition to the shifted field. Another group of birds was trained to solve the orientation task, but with visual landmarks as directional cue. The birds were then tested for their orientation performance in the same magnetic conditions as applied for the first experiment. Results The zebra finches could be trained successfully to orient in the geomagnetic field for food search in the north/south axis. They were also well oriented in test condition 1, with the magnetic field shifted horizontally by 90 degrees. In contrast, when the oscillating field was added the directional choices during food search were randomly distributed. Birds that were trained to visually guided orientation showed no difference of orientation performance in the two magnetic conditions.
Background: The Radical-Pair-Model postulates that the reception of magnetic compass directions in birds is based on spin-chemical reactions in specialized photopigments in the eye, with cryptochromes discussed as candidate molecules. But so far, the exact subcellular characterization of these molecules in the retina remained unknown. Methodology/Principal Findings: We here describe the localization of cryptochrome 1a (Cry1a) in the retina of European robins, Erithacus rubecula, and domestic chickens, Gallus gallus, two species that have been shown to use the magnetic field for compass orientation. In both species, Cry1a is present exclusively in the ultraviolet/violet (UV/V) cones that are distributed across the entire retina. Electron microscopy shows Cry1a in ordered bands along the membrane discs of the outer segment, and cell fractionation reveals Cry1a in the membrane fraction, suggesting the possibility that Cry1a is anchored along membranes. Conclusions/Significance: We provide first structural evidence that Cry1a occurs within a sensory structure arranged in a way that fulfils essential requirements of the Radical-Pair-Model. Our findings, identifying the UV/V-cones as probable magnetoreceptors, support the assumption that Cry1a is indeed the receptor molecule mediating information on magnetic directions, and thus provide the Radical-Pair-Model with a profound histological background.
Cryptochrome 1a, located in the UV/violet-sensitive cones in the avian retina, is discussed as receptor molecule for the magnetic compass of birds. Our previous immunohistochemical studies of chicken retinae with an antiserum that labelled only activated cryptochrome 1a had shown activation of cryptochrome 1a under 373 nm UV, 424 nm blue, 502 nm turquoise and 565 nm green light. Green light, however, does not allow the first step of photoreduction of oxidized cryptochromes to the semiquinone. As the chickens had been kept under ‘white’ light before, we suggested that there was a supply of the semiquinone present at the beginning of the exposure to green light, which could be further reduced and then re-oxidized. To test this hypothesis, we exposed chickens to various wavelengths (1) for 30 min after being kept in daylight, (2) for 30 min after a 30 min pre-exposure to total darkness, and (3) for 1 h after being kept in daylight. In the first case, we found activated cryptochrome 1a under UV, blue, turquoise and green light; in the second two cases we found activated cryptochrome 1a only under UV to turquoise light, where the complete redox cycle of cryptochrome can run, but not under green light. This observation is in agreement with the hypothesis that activated cryptochrome 1a is found as long as there is some of the semiquinone left, but not when the supply is depleted. It supports the idea that the crucial radical pair for magnetoreception is generated during re-oxidation.
The radical pair model proposes that the avian magnetic compass is based on radical pair processes in the eye, with cryptochrome, a flavoprotein, suggested as receptor molecule. Cryptochrome 1a (Cry1a) is localized at the discs of the outer segments of the UV/violet cones of European robins and chickens. Here, we show the activation characteristics of a bird cryptochrome in vivo under natural conditions. We exposed chickens for 30 min to different light regimes and analysed the amount of Cry1a labelled with an antiserum against an epitope at the C-terminus of this protein. The staining after exposure to sunlight and to darkness indicated that the antiserum labels only an illuminated, activated form of Cry1a. Exposure to narrow-bandwidth lights of various wavelengths revealed activated Cry1a at UV, blue and turquoise light. With green and yellow, the amount of activated Cry1a was reduced, and with red, as in the dark, no activated Cry1a was labelled. Activated Cry1a is thus found at all those wavelengths at which birds can orient using their magnetic inclination compass, supporting the role of Cry1a as receptor molecule. The observation that activated Cry1a and well-oriented behaviour occur at 565 nm green light, a wavelength not absorbed by the fully oxidized form of cryptochrome, suggests that a state other than the previously suggested Trp/FAD radical pair formed during photoreduction is crucial for detecting magnetic directions.
Cryptochromes, blue-light absorbing proteins involved in the circadian clock, have been proposed to be the receptor molecules of the avian magnetic compass. In birds, several cryptochromes occur: Cryptochrome 2, Cryptochrome 4 and two splice products of Cryptochrome 1, Cry1a and Cry1b. With an antibody not distinguishing between the two splice products, Cryptochrome 1 had been detected in the retinal ganglion cells of garden warblers during migration. A recent study located Cry1a in the outer segments of UV/V-cones in the retina of domestic chickens and European robins, another migratory species. Here we report the presence of cryptochrome 1b (eCry1b) in retinal ganglion cells and displaced ganglion cells of European Robins, Erithacus rubecula. Immuno histochemistry at the light microscopic and electron microscopic level showed eCry1b in the cell plasma, free in the cytosol as well as bound to membranes. This is supported by immuno blotting. However, this applies only to robins in the migratory state. After the end of the migratory phase, the amount of eCry1b was markedly reduced and hardly detectable. In robins, the amount of eCry1b in the retinal ganglion cells varies with season: it appears to be strongly expressed only during the migratory period when the birds show nocturnal migratory restlessness. Since the avian magnetic compass does not seem to be restricted to the migratory phase, this seasonal variation makes a role of eCry1b in magnetoreception rather unlikely. Rather, it could be involved in physiological processes controlling migratory restlessness and thus enabling birds to perform their nocturnal flights.