Peter Thalau

Resonance effects indicate a radical-pair mechanism for avian magnetic compass

Migratory birds are known to use the geomagnetic field as a source of compass information. There are two competing hypotheses for the primary process underlying the avian magnetic compass, one involving magnetite, the other a magnetically sensitive chemical reaction. Here we show that oscillating magnetic fields disrupt the magnetic orientation behaviour of migratory birds. Robins were disoriented when exposed to a vertically aligned broadband (0.1–10 MHz) or a single-frequency (7-MHz) field in addition to the geomagnetic field. Moreover, in the 7-MHz oscillating field, this effect depended on the angle between the oscillating and the geomagnetic fields. The birds exhibited seasonally appropriate migratory orientation when the oscillating field was parallel to the geomagnetic field, but were disoriented when it was presented at a 24° or 48° angle. These results are consistent with a resonance effect on singlet–triplet transitions and suggest a magnetic compass based on a radical-pair mechanism.

A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons

Animals make use of the Earth’s magnetic field for navigation and regulation of vegetative functions; however, the anatomical and physiological basis for the magnetic sense has not been elucidated yet. Our recent results from histology and X-ray analyses support the hypothesis that delicate iron-containing structures in the skin of the upper beak of homing pigeons might serve as a biological magnetometer. Histology has revealed various iron sites within dendrites of the trigeminal nerve, their arrangement along strands of axons, the existence of three dendritic fields in each side of the beak with specific 3D-orientations, and the bilateral symmetry of the whole system. Element mapping by micro-synchrotron X-ray fluorescence analysis has shown the distribution of iron and its quantities. Micro-synchrotron X-ray absorption near-edge-structure spectroscopy has allowed us to unambiguously identify maghemite as the predominating iron mineral (90 vs 10% magnetite). In this paper, we show that iron-based magnetoreception needs the presence of both of these iron minerals, their specific dimensions, shapes, and arrangements in three different subcellular compartments. We suggest that an inherent magnetic enhancement process via an iron-crusted vesicle and the attached chains of iron platelets might be sufficient to account for the sensitivity and specificity required by such a magnetoreceptor. The appropriate alignment between the Earth’s magnetic field and the maghemite bands would induce a multiple attraction of the magnetite bullets perpendicular to the membrane, thus, triggering strain-sensitive membrane channels and a primary receptor potential. Due to its 3D architecture and physicochemical nature, the dendritic system should be able to separately sense the three vector components of the Earth’s local field, simultaneously—allowing birds to detect their geographic position by the magnetic vector, i.e., amplitude and direction of the local magnetic field, irrespective of the animal’s posture or movement and photoreception.

Directional orientation of birds by the magnetic field under different light conditions.

This paper reviews the directional orientation of birds with the help of the geomagnetic field under various light conditions. Two fundamentally different types of response can be distinguished. (i) Compass orientation controlled by the inclination compass that allows birds to locate courses of different origin. This is restricted to a narrow functional window around the total intensity of the local geomagnetic field and requires light from the short-wavelength part of the spectrum. The compass is based on radical-pair processes in the right eye; magnetite-based receptors in the beak are not involved. Compass orientation is observed under ‘white’ and low-level monochromatic light from ultraviolet (UV) to about 565 nm green light. (ii) ‘Fixed direction’ responses occur under artificial light conditions such as more intense monochromatic light, when 590 nm yellow light is added to short-wavelength light, and in total darkness. The manifestation of these responses depends on the ambient light regime and is ‘fixed’ in the sense of not showing the normal change between spring and autumn; their biological significance is unclear. In contrast to compass orientation, fixed-direction responses are polar magnetic responses and occur within a wide range of magnetic intensities. They are disrupted by local anaesthesia of the upper beak, which indicates that the respective magnetic information is mediated by iron-based receptors located there. The influence of light conditions on the two types of response suggests complex interactions between magnetoreceptors in the right eye, those in the upper beak and the visual system.

Avian Magnetoreception: Elaborate Iron Mineral Containing Dendrites in the Upper Beak Seem to Be a Common Feature of Birds

The magnetic field sensors enabling birds to extract orientational information from the Earths magnetic field have remained enigmatic. Our previously published results from homing pigeons have made us suggest that the iron containing sensory dendrites in the inner dermal lining of the upper beak are a candidate structure for such an avian magnetometer system. Here we show that similar structures occur in two species of migratory birds (garden warbler, Sylvia borin and European robin, Erithacus rubecula) and a non-migratory bird, the domestic chicken (Gallus gallus). In all these bird species, histological data have revealed dendrites of similar shape and size, all containing iron minerals within distinct subcellular compartments of nervous terminals of the median branch of the Nervus ophthalmicus. We also used microscopic X-ray absorption spectroscopy analyses to identify the involved iron minerals to be almost completely Fe III-oxides. Magnetite (Fe II/III) may also occur in these structures, but not as a major Fe constituent. Our data suggest that this complex dendritic system in the beak is a common feature of birds, and that it may form an essential sensory basis for the evolution of at least certain types of magnetic field guided behavior.

The magnetic compass mechanisms of birds and rodents are based on different physical principles

Recently, oscillating magnetic fields in the MHz-range were introduced as a useful diagnostic tool to identify the mechanism underlying magnetoreception. The effect of very weak high-frequency fields on the orientation of migratory birds indicates that the avian magnetic compass is based on a radical pair mechanism. To analyse the nature of the magnetic compass of mammals, we tested rodents, Ansells mole-rats, using their tendency to build their nests in the southern part of the arena as a criterion whether or not they could orient. In contrast to birds, their orientation was not disrupted when a broad-band field of 0.1–10 MHz of 85 nT or a 1.315 MHz field of 480 nT was added to the static geomagnetic field of 46 000 nT. Even increasing the intensity of the 1.315 MHz field (Zeeman frequency in the local geomagnetic field) to 4800 nT, more than a tenth of the static field, the mole-rats remained unaffected and continued to build their nests in the south. These results indicate that in contrast to that of birds, their magnetic compass does not involve radical pair processes; it seems to be based on a fundamentally different principle, which probably involves magnetite.

Oscillating magnetic field disrupts magnetic orientation in Zebra finches, Taeniopygia guttata.

BackgroundZebra 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.MethodsIn 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.ResultsThe 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.ConclusionThe results indicate that zebra finches use a receptor that bases on radical pair processes for sensing the direction of the earth magnetic field in this short distance orientation behavior.

Magnetoreception in birds: different physical processes for two types of directional responses.

Migratory orientation in birds involves an inclination compass based on radical‐pair processes. Under certain light regimes, however, “fixed‐direction” responses are observed that do not undergo the seasonal change between spring and autumn typical for migratory orientation. To identify the underlying transduction mechanisms, we analyzed a fixed‐direction response under a combination of 502 nm turquoise and 590 nm yellow light, with migratory orientation under 565 nm green light serving as the control. High‐frequency fields, diagnostic for a radical‐pair mechanism, disrupted migratory orientation without affecting fixed‐direction responses. Local anaesthesia of the upper beak where magnetite is found in birds, in contrast, disrupted the fixed‐direction response without affecting migratory orientation. The two types of responses are thus based on different physical principles, with the compass response based on a radical pair mechanism and the fixed‐direction responses probably originating in magnetite‐bas...

Avian magnetic compass can be tuned to anomalously low magnetic intensities

The avian magnetic compass works in a fairly narrow functional window around the intensity of the local geomagnetic field, but adjusts to intensities outside this range when birds experience these new intensities for a certain time. In the past, the geomagnetic field has often been much weaker than at present. To find out whether birds can obtain directional information from a weak magnetic field, we studied spontaneous orientation preferences of migratory robins in a 4 µT field (i.e. a field of less than 10 per cent of the local intensity of 47 µT). Birds can adjust to this low intensity: they turned out to be disoriented under 4 µT after a pre-exposure time of 8 h to 4 µT, but were able to orient in this field after a total exposure time of 17 h. This demonstrates a considerable plasticity of the avian magnetic compass. Orientation in the 4 µT field was not affected by local anaesthesia of the upper beak, but was disrupted by a radiofrequency magnetic field of 1.315 MHz, 480 nT, suggesting that a radical-pair mechanism still provides the directional information in the low magnetic field. This is in agreement with the idea that the avian magnetic compass may have developed already in the Mesozoic in the common ancestor of modern birds.

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

SUMMARY 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.