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Birds can use two kinds of information from the geomagnetic field for navigation: the direction of the field lines as a compass and probably magnetic intensity as a component of the navigational 'map'. The direction of the magnetic field appears to be sensed via radical pair processes in the eyes, with the crucial radical pairs formed by cryptochrome. It is transmitted by the optic nerve to the brain, where parts of the visual system seem to process the respective information. Magnetic intensity appears to be perceived by magnetite-based receptors in the beak region; the information is transmitted by the ophthalmic branch of the trigeminal nerve to the trigeminal ganglion and the trigeminal brainstem nuclei. Yet in spite of considerable progress in recent years, many details are still unclear, among them details of the radical pair processes and their transformation into a nervous signal, the precise location of the magnetite-based receptors and the centres in the brain where magnetic information is combined with other navigational information for the navigational processes.

The avian magnetic inclination compass is based on radical pair processes, with cryptochrome (Cry) assumed to form the crucial radical pairs; it requires short-wavelength light from UV to green. Under high-intensity narrow-band lights and when yellow light is added, the magnetic compass is disrupted: migratory birds no longer prefer their migratory direction, but show other orientation responses. The candidate receptor molecule Cry1a is located in the shortwavelength-sensitive SWS1 cone photoreceptors in the retina. The present analysis of avian retinae after the respective illuminations showed that no activated Cry1a was present under 565 nm green light of medium and high intensity, and hardly any under high intensity 502 nm turquoise, whereas we found activated Cry1a at all three tested intensities of 373 nm UV and 424 nm blue light. Activated Cry1a also was found when 590 nm yellow light was added to low-intensity light of the four colors; yet these light combinations result in impaired magnetic orientation. This indicates that the disruption of the magnetic compass does not occur at the receptor level in the retina, but at higher processing stages, where the unnatural, almost monochromatic or bichromatic illumination causes yet unknown responses that interfere with the inclination compass.

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., (© 2016 The Authors.)

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., (© 2014 The Author(s) Published by the Royal Society. All rights reserved.)

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., (© 2014. Published by The Company of Biologists Ltd.)

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., (© 2014. Published by The Company of Biologists Ltd.)

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.

In previous conditioning experiments training domestic chickens to magnetic directions, a brown strain solved the task, whereas a white strain seemed unable to do so (Freire et al. Anim Cogn 11:547-552, 2008). To test whether this was possibly caused by loss of magnetic compass orientation in the white chickens, we analyzed the distribution of cryptochrome 1a, the candidate receptor molecule mediating magnetic compass information, in the retinae of Lohmann Browns and White Leghorns and found no difference between the two strains. Yet, subsequent training experiments replicated the former findings: Lohmann Browns used the magnetic field to find an imprinting stimulus hidden behind the screen in a specific magnetic direction, whereas White Leghorns did not solve the task. However, when we altered the training method by training also in a magnetic field with North shifted to geographic East and including a punishment for incorrect choices, the performance of White Leghorns improved to a significant preference for the expected directions. The Lohmann Browns, on the other hand, seemed frightened and chose randomly. Our results thus demonstrate the crucial role of the training method for conditioning to magnetic stimuli, with differences found even between strains of the same species.

Iron-rich structures have been described in the beak of homing pigeons, chickens and several species of migratory birds and interpreted as magnetoreceptors. Here, we will briefly review findings associated with these receptors that throw light on their nature, their function and their role in avian navigation. Electrophysiological recordings from the ophthalmic nerve, behavioral studies and a ZENK-study indicate that the trigeminal system, the nerves innervating the beak, mediate information on magnetic changes, with the electrophysiological study suggesting that these are changes in intensity. Behavioral studies support the involvement of magnetite and the trigeminal system in magnetoreception, but clearly show that the inclination compass normally used by birds represents a separate system. However, if this compass is disrupted by certain light conditions, migrating birds show 'fixed direction' responses to the magnetic field, which originate in the receptors in the beak. Together, these findings point out that there are magnetite-based magnetoreceptors located in the upper beak close to the skin. Their natural function appears to be recording magnetic intensity and thus providing one component of the multi-factorial 'navigational map' of birds.

Animals can use the direction of the magnetic field as a compass and the intensity of the magnetic field as a component of the navigational 'map'. Two fundamentally different mechanisms of magnetoreception have been discussed: (1) light-dependent reactions in specialized photopigments lead to radical pairs, with the ratio singlet/ triplet depending on the molecule's alignment with respect to the ambient magnetic field and (2) reactions involving small crystals of magnetite, a specific iron oxide of biogen origin. The first mechanism provides birds and possibly amphibians and insects with compass information; the second, which can theoretically provide animals with information on direction and intensity, appears to mediate intensity information in birds and compass information e.g., in mammals. Little is known about the magnetoreception mechanisms in other animals.

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.