Mathematical analysis of the homing flights of pigeons based on GPS tracks.

To analyse the effect of magnetic and olfactory deprivation on the homing flight of pigeons, we released birds from a familiar site with either their upper beak or their nostrils anaesthetized. The tracks were analysed by time lag embedding to calculate the short-term correlation dimension, a variable that reflects the degrees of freedom and thus the number of factors involved in a system. We found that higher natural fluctuations in the earth's magnetic field characterized by A P-indices of 8 and above caused a reduction of the correlation dimension of the control birds. We thus separated the data into two groups according to whether they were recorded on magnetically quiet days or on days with higher magnetic fluctuations. Anaesthetizing the upper beak had no significant effect. Making pigeons anosmic reduced the correlation dimension on magnetically quiet days, but did not cause any reduction on days with higher fluctuations. Altogether, our data suggest an involvement of magnetic cues and olfactory factors during the homing flight and point to a robust, multi-factorial map.

Light-dependent magnetoreception in birds: the crucial step occurs in the dark.

The Radical Pair Model proposes that the avian magnetic compass is based on spin-chemical processes: since the ratio between the two spin states singlet and triplet of radical pairs depends on their alignment in the magnetic field, it can provide information on magnetic directions. Cryptochromes, blue light-absorbing flavoproteins, with flavin adenine dinucleotide as chromophore, are suggested as molecules forming the radical pairs underlying magnetoreception. When activated by light, cryptochromes undergo a redox cycle, in the course of which radical pairs are generated during photo-reduction as well as during light-independent re-oxidation. This raised the question as to which radical pair is crucial for mediating magnetic directions. Here, we present the results from behavioural experiments with intermittent light and magnetic field pulses that clearly show that magnetoreception is possible in the dark interval, pointing to the radical pair formed during flavin re-oxidation. This differs from the mechanism considered for cryptochrome signalling the presence of light and rules out most current models of an avian magnetic compass based on the radical pair generated during photo-reduction. Using the radical pair formed during re-oxidation may represent a specific adaptation of the avian magnetic compass.

Magnetoreception in birds: the effect of radio-frequency fields.

The avian magnetic compass, probably based on radical pair processes, works only in a narrow functional window around the local field strength, with cryptochrome 1a as most likely receptor molecule. Radio-frequency fields in the MHz range have been shown to disrupt the birds' orientation, yet the nature of this interference is still unclear. In an immuno-histological study, we tested whether the radio-frequency fields interfere with the photoreduction of cryptochrome, but this does not seem to be the case. In behavioural studies, birds were not able to adjust to radio-frequency fields like they are able to adjust to static fields outside the normal functional range: neither a 2-h pre-exposure in a 7.0 MHz field, 480 nT, nor a 7-h pre-exposure in a 1.315 MHz field, 15 nT, allowed the birds to regain their orientation ability. This inability to adjust to radio-frequency fields suggests that these fields interfere directly with the primary processes of magnetoreception and therefore disable the avian compass as long as they are present. They do not have lasting adverse after-effects, however, as birds immediately after exposure to a radio-frequency field were able to orient in the local geomagnetic field.

Magnetoreception in birds: II. Behavioural experiments concerning the cryptochrome cycle.

Behavioural tests of the magnetic compass of birds and corresponding immunohistological studies on the activation of retinal cryptochrome 1a, the putative receptor molecule, showed oriented behaviour and activated Cry1a under 373 nm UV, 424 nm blue, 502 nm turquoise and 565 nm green light, although the last wavelength does not allow the first step of photoreduction of cryptochrome to the semiquinone form. The tested birds had been kept under 'white' light before, hence we suggested that there was a supply of semiquinone present at the beginning of the exposure to green light that could be further reduced and then re-oxidized. To test the hypothesis in behavioural experiments, we tested robins, Erithacus rubecula, under various wavelengths (1) after 1 h pre-exposure to total darkness and (2) after 1 h pre-exposure to the same light as used in the test. The birds were oriented under blue and turquoise light, where the full cryptochrome cycle can run, but not under green light. This finding is in agreement with the hypothesis. Orientation under green light appears to be a transient phenomenon until the supply of semiquinone is depleted.

Interactions between the visual and the magnetoreception system: different effects of bichromatic light regimes on the directional behavior of migratory birds.

When magnetic compass orientation of migratory robins was tested, the birds proved well oriented under low intensity monochromatic light of shorter wavelengths up to 565 nm green; from 583 nm yellow onward, they were disoriented. In the present study, we tested robins under bichromatic lights composed (1) of 424 nm blue and 565 nm green and (2) of 565 nm green and 583 nm yellow at two intensities. Under dim blue-green light with a total quantal flux of ca. 8 × 10(15)quanta/sm(2), the birds were well oriented in their migratory direction by their inclination compass; under blue-green light of twice this intensity, their orientation became axial. In both cases, the magnetic directional information was mediated by the radical pair processes in the eye. When green and yellow light were combined, however, the nature of the behavior changed. Under green-yellow light of the higher intensity, the birds showed a 'fixed direction' response that was polar, no longer controlled by the normal inclination compass; under dim green-yellow light, the response became axial. Under these two light conditions, the respective directional information was mediated by the magnetite-based receptors in the skin of the upper beak. Apparently, yellow light leads to a change from one magnetoreception system to the other. How this change is effected is still unknown; it appears to reflect complex interactions between the visual and the two magnetoreception systems.

Development of lateralization of the magnetic compass in a migratory bird.

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.

Magnetic orientation of migratory robins, Erithacus rubecula, under long-wavelength light.

The avian magnetic compass is an inclination compass that appears to be based on radical pair processes. It requires light from the short-wavelength range of the spectrum up to 565 nm green light; under longer wavelengths, birds are disoriented. When pre-exposed to longer wavelengths for 1 h, however, they show oriented behavior. This orientation is analyzed under 582 nm yellow light and 645 nm red light in the present study: while the birds in spring prefer northerly directions, they do not show southerly tendencies in autumn. Inversion of the vertical component does not have an effect whereas reversal of the horizontal component leads to a corresponding shift, indicating that a polar response to the magnetic field is involved. Oscillating magnetic fields in the MHz range do not affect the behavior but anesthesia of the upper beak causes disorientation. This indicates that the magnetic information is no longer provided by the radical pair mechanism in the eye but by the magnetite-based receptors in the skin of the beak. Exposure to long-wavelength light thus does not expand the spectral range in which the magnetic compass operates but instead causes a different mechanism to take over and control orientation.

Interaction of magnetite-based receptors in the beak with the visual system underlying 'fixed direction' responses in birds.

BACKGROUND: European robins, Erithacus rubecula, show two types of directional responses to the magnetic field: (1) compass orientation that is based on radical pair processes and lateralized in favor of the right eye and (2) so-called 'fixed direction' responses that originate in the magnetite-based receptors in the upper beak. Both responses are light-dependent. Lateralization of the 'fixed direction' responses would suggest an interaction between the two magnetoreception systems. RESULTS: Robins were tested with either the right or the left eye covered or with both eyes uncovered for their orientation under different light conditions. With 502 nm turquoise light, the birds showed normal compass orientation, whereas they displayed an easterly 'fixed direction' response under a combination of 502 nm turquoise with 590 nm yellow light. Monocularly right-eyed birds with their left eye covered were oriented just as they were binocularly as controls: under turquoise in their northerly migratory direction, under turquoise-and-yellow towards east. The response of monocularly left-eyed birds differed: under turquoise light, they were disoriented, reflecting a lateralization of the magnetic compass system in favor of the right eye, whereas they continued to head eastward under turquoise-and-yellow light. CONCLUSION: 'Fixed direction' responses are not lateralized. Hence the interactions between the magnetite-receptors in the beak and the visual system do not seem to involve the magnetoreception system based on radical pair processes, but rather other, non-lateralized components of the visual system.