The magnetite-based receptors in the beak of birds and their role in avian navigation

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

Magnetite-based magnetoreception in birds: the effect of a biasing field and a pulse on migratory behavior

To test the hypothesis that single domain magnetite is involved in magnetoreception, we treated Australian silvereyes Zosterops l. lateralis with a strong, brief pulse designed to alter the magnetization of single domain particles. This pulse was administered in the presence of a 1 mT biasing field, either parallel to the direction of the biasing field (PAR group) or antiparallel (ANTI group). In the case of magnetoreceptors based on freely moving single domain particles, the PAR treatment should have little effect, whereas the ANTI treatment should cause remagnetization of the magnetite particles involved in a receptor and could produce a maximum change in that receptor's output for some receptor configurations. Migratory orientation was used as a criterion to assess the effect on the receptor. Before treatment, both groups preferred their normal northerly migratory direction. Exposure to the biasing field alone did not affect their behavior. Treatment with the pulse in the presence of the biasing field caused both the PAR and the ANTI birds to show an axial preference for the east—west axis, with no difference between the two groups. Although these results are in accordance with magnetite-based magnetoreceptors playing a role in migratory orientation, they do not support the hypothesis that single domains in polarity-sensitive receptors are free to move through all solid angles. Possible interpretations, including other arrangements of single domains and superparamagnetic crystals, are discussed

Sensing Magnetic Directions in Birds: Radical Pair Processes Involving Cryptochrome

Birds can use the geomagnetic field for compass orientation. Behavioral experiments, mostly with migrating passerines, revealed three characteristics of the avian magnetic compass: (1) it works spontaneously only in a narrow functional window around the intensity of the ambient magnetic field, but can adapt to other intensities, (2) it is an “inclination compass”, not based on the polarity of the magnetic field, but the axial course of the field lines, and (3) it requires short-wavelength light from UV to 565 nm Green. The Radical Pair-Model of magnetoreception can explain these properties by proposing spin-chemical processes in photopigments as underlying mechanism. Applying radio frequency fields, a diagnostic tool for radical pair processes, supports an involvement of a radical pair mechanism in avian magnetoreception: added to the geomagnetic field, they disrupted orientation, presumably by interfering with the receptive processes. Cryptochromes have been suggested as receptor molecules. Cry1a is found in the eyes of birds, where it is located at the membranes of the disks in the outer segments of the UV-cones in chickens and robins. Immuno-histochemical studies show that it is activated by the wavelengths of light that allow magnetic compass orientation in birds

Light-dependent magnetoreception in birds: increasing intensity of monochromatic light changes the nature of the response

BACKGROUND: The Radical Pair model proposes that magnetoreception is a light-dependent process. Under low monochromatic light from the short-wavelength part of the visual spectrum, migratory birds show orientation in their migratory direction. Under monochromatic light of higher intensity, however, they showed unusual preferences for other directions or axial preferences. To determine whether or not these responses are still controlled by the respective light regimes, European robins, Erithacus rubecula, were tested under UV, Blue, Turquoise and Green light at increasing intensities, with orientation in migratory direction serving as a criterion whether or not magnetoreception works in the normal way. RESULTS: The birds were well oriented in their seasonally appropriate migratory direction under 424 nm Blue, 502 nm Turquoise and 565 nm Green light of low intensity with a quantal flux of 8·10(15 )quanta s(-1 )m(-2), indicating unimpaired magnetoreception. Under 373 nm UV of the same quantal flux, they were not oriented in migratory direction, showing a preference for the east-west axis instead, but they were well oriented in migratory direction under UV of lower intensity. Intensities of above 36·10(15 )quanta s(-1 )m(-2 )of Blue, Turquoise and Green light elicited a variety of responses: disorientation, headings along the east-west axis, headings along the north-south axis or 'fixed' direction tendencies. These responses changed as the intensity was increased from 36·10(15 )quanta s(-1 )m(-2 )to 54 and 72·10(15 )quanta s(-1 )m(-2). CONCLUSION: The specific manifestation of responses in directions other than the migratory direction clearly depends on the ambient light regime. This implies that even when the mechanisms normally providing magnetic compass information seem disrupted, processes that are activated by light still control the behavior. It suggests complex interactions between different types of receptors, magnetic and visual. The nature of the receptors involved and details of their connections are not yet known; however, a role of the color cones in the processes mediating magnetic input is suggested

Flight tracks of homing pigeons measured with GPS

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

Avian magnetic compass can be tuned to anomalously low magnetic intensities

The avian magnetic compass works in a fairly narrow functional windowaround the intensity of the local geomagnetic field, but adjusts tointensities outside this range when birds experience these newintensities for a certain time. In the past, the geomagnetic field hasoften been much weaker than at present. To find out whether birds canobtain directional information from a weak magnetic field, we studiedspontaneous orientation preferences of migratory robins in a 4 mu Tfield (i.e. a field of less than 10 per cent of the local intensity of47 mu T). Birds can adjust to this low intensity: they turned out to bedisoriented under 4 mu T after a pre-exposure time of 8 h to 4 mu T, butwere able to orient in this field after a total exposure time of 17 h.This demonstrates a considerable plasticity of the avian magneticcompass. Orientation in the 4 mu T field was not affected by localanaesthesia of the upper beak, but was disrupted by a radiofrequencymagnetic field of 1.315 MHz, 480 nT, suggesting that a radical-pairmechanism still provides the directional information in the low magneticfield. This is in agreement with the idea that the avian magneticcompass may have developed already in the Mesozoic in the commonancestor of modern birds

Magnetic orientation and magnetoreception in birds and other animals

Abstract Animals use the geomagnetic field in many ways: the magnetic vector provides a compass; magnetic intensity and/or inclination play a role as a component of the navigational 'map', and magnetic conditions of certain regions act as 'sign posts' or triggers, eliciting specific responses. A magnetic compass is widespread among animals, magnetic navigation is indicated e.g. in birds, marine turtles and spiny lobsters and the use of magnetic 'sign posts' has been described for birds and marine turtles. For magnetoreception, two hypotheses are currently discussed, one proposing a chemical compass based on a radical pair mechanism, the other postulating processes involving magnetite particles. The available evidence suggests that birds use both mechanisms, with the radical pair mechanism in the right eye providing directional information and a magnetitebased mechanism in the upper beak providing information on position as component of the 'map'. Behavioral data from other animals indicate a lightdependent compass probably based on a radical pair mechanism in amphibians and a possibly magnetitebased mechanism in mammals. Histological and electrophysiological data suggest a magnetite-based mechanism in the nasal cavities of salmonid fish. Little is known about the parts of the brain where the respective information is processed

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

The GPS flight recorder for homing pigeons works : design and first results

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

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