Orientation of migratory birds under ultraviolet light.

In view of the finding that cryptochrome 1a, the putative receptor molecule for the avian magnetic compass, is restricted to the ultraviolet single cones in European Robins, we studied the orientation behaviour of robins and Australian Silvereyes under monochromatic ultraviolet (UV) light. At low intensity UV light of 0.3 mW/m(2), birds showed normal migratory orientation by their inclination compass, with the directional information originating in radical pair processes in the eye. At 2.8 mW/m(2), robins showed an axial preference in the east-west axis, whereas silvereyes preferred an easterly direction. At 5.7 mW/m(2), robins changed direction to a north-south axis. When UV light was combined with yellow light, robins showed easterly 'fixed direction' responses, which changed to disorientation when their upper beak was locally anaesthetised with xylocaine, indicating that they were controlled by the magnetite-based receptors in the beak. Orientation under UV light thus appears to be similar to that observed under blue, turquoise and green light, albeit the UV responses occur at lower light levels, probably because of the greater light sensitivity of the UV cones. The orientation under UV light and green light suggests that at least at the level of the retina, magnetoreception and vision are largely independent of each other.

Magnetoreception: activated cryptochrome 1a concurs with magnetic orientation in birds.

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.

Magnetoreception of directional information in birds requires nondegraded vision.

The magnetic compass orientation of birds is light dependent. The respective directional information, originating in radical pair processes, is mediated by the right eye. These findings suggest possible interactions between magnetoreception and vision, in particular with the perception of contours, because the right eye has been found to be dominant in discrimination tasks requiring object vision. Here we report tests in the local geomagnetic field with European robins wearing goggles equipped with a clear and a frosted foil of equal translucence of 70%. Robins with a clear foil on the right eye and a frosted foil on the left eye oriented in the migratory direction as well as birds using both eyes. Birds with a frosted foil that blurred vision on the right eye and a clear foil on the left eye, in contrast, were disoriented. These findings are the first to show that avian magnetoreception requires, in addition to light, a nondegraded image formation along the projectional streams of the right retina. This suggests crucial interactions between the processing of visual pattern information and the conversion of magnetic input into directional information.

Magnetoreception in birds: no intensity window in "fixed direction" responses.

Under 502 nm turquoise light combined with 590 nm yellow light and in total darkness, European robins, Erithacus rubecula, no longer prefer their migratory direction, but exhibit so-called fixed direction responses that do not show the seasonal change between spring and autumn. We tested robins under these light conditions in the local geomagnetic field of 46 microT, a field of twice this intensity, 92 microT, and a field of three times this intensity, 138 microT. Under all three magnetic conditions, the birds preferred the same easterly direction under turquoise-and-yellow light and the same northwesterly direction under dark, while they were oriented in their seasonally appropriate direction under control conditions. "Fixed direction" responses are thus not limited to a narrow intensity window as has been found for normal compass orientation. This can be attributed to their origin in the magnetite-based receptor in the upper beak, which operates according to fundamentally different principles than the radical pair mechanism in the retina mediating compass orientation. "Fixed direction" responses are possibly a relict of a receptor mechanism that changed its function, now mainly providing information on magnetic intensity.

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.

Magnetic compass of birds is based on a molecule with optimal directional sensitivity.

The avian magnetic compass has been well characterized in behavioral tests: it is an "inclination compass" based on the inclination of the field lines rather than on the polarity, and its operation requires short-wavelength light. The "radical pair" model suggests that these properties reflect the use of specialized photopigments in the primary process of magnetoreception; it has recently been supported by experimental evidence indicating a role of magnetically sensitive radical-pair processes in the avian magnetic compass. In a multidisciplinary approach subjecting migratory birds to oscillating fields and using their orientation responses as a criterion for unhindered magnetoreception, we identify key features of the underlying receptor molecules. Our observation of resonance effects at specific frequencies, combined with new theoretical considerations and calculations, indicate that birds use a radical pair with special properties that is optimally designed as a receptor in a biological compass. This radical pair design might be realized by cryptochrome photoreceptors if paired with molecular oxygen as a reaction partner.

Light-dependent magnetoreception: orientation behaviour of migratory birds under dim red light.

Magnetic compass orientation in migratory birds has been shown to be based on radical pair processes and to require light from the short wavelength part of the spectrum up to 565 nm Green. Under dim red light of 645 nm wavelength and 1 mW m(-2) intensity, Australian silvereyes and European robins showed a westerly tendency that did not change between spring and autumn, identifying it as a 'fixed direction' response. A thorough analysis revealed that this orientation did not involve the inclination compass, but was a response based on the polarity of the magnetic field. Furthermore, in contrast to the orientation under short-wavelength light, it could be disrupted by local anaesthesia of the upper beak where iron-containing receptors are located, indicating that it is controlled by these receptors. The similarity of the response under dim red light to the response in total darkness suggests that the two responses may be identical. These findings indicate that the observed 'fixed direction' response under dim red light is fundamentally different from the normal compass orientation, which is based on radical pair processes.

Orientation of birds in total darkness.

Magnetic compass orientation of migratory birds is known to be light dependent, and radical-pair processes have been identified as the underlying mechanism. Here we report for the first time results of tests with European robins, Erithacus rubecula, in total darkness and, as a control, under 565 nm green light. Under green light, the robins oriented in their normal migratory direction, with southerly headings in autumn and northerly headings in spring. By contrast, in darkness they significantly preferred westerly directions in spring as well as autumn. This failure to show the normal seasonal change characterizes the orientation in total darkness as a "fixed direction" response. Tests in magnetic fields with the vertical or the horizontal component inverted showed that the preferred direction depended on the magnetic field but did not involve the avian inclination compass. A high-frequency field of 1.315 MHz did not affect the behavior, whereas local anesthesia of the upper beak resulted in disorientation. The behavior in darkness is thus fundamentally different from normal compass orientation and relies on another source of magnetic information: It does not involve the radical-pair mechanism but rather originates in the iron-containing receptors in the upper beak.

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 x 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 x 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 x 10(15) quanta s(-1) m(-2) to 54 and 72 x 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.

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-based receptors in the upper beak. Directional input from these receptors seems to affect the behavior only when the regular inclination compass does not work properly. Evolutionary considerations suggest that magnetite-based receptors may represent an ancient mechanism that, in birds, has been replaced by the modern inclination compass based on radical-pair processes now used for directional orientation.

Avian magnetic compass: fast adjustment to intensities outside the normal functional window.

To determine how fast birds can adapt to magnetic intensities outside the normal functional window of their magnetic compass, we tested migratory birds in a magnetic field of 92,000 nT, twice the intensity of the local geomagnetic field at the test site in Frankfurt a.M., Germany. In the local field, robins showed a significant preference of their southerly migratory direction, whereas in the 92,000-nT field, they were initially disoriented. However, when the birds were preexposed to 92,000 nT for 1 h before being tested, they were able to orient under this intensity, and their behavior did not differ from that in the geomagnetic field. These data show that birds require only a short time to adjust to magnetic intensities, which they cannot spontaneously use for orientation. Interpreting these findings in view of the radical pair model (Ritz et al. 2000), this means that they can learn rather quickly to interpret novel activation patterns on their retina.

Two different types of light-dependent responses to magnetic fields in birds.

A model of magnetoreception proposes that the avian magnetic compass is based on a radical pair mechanism, with photon absorption leading to the formation of radical pairs. Analyzing the predicted light dependency by testing migratory birds under monochromatic lights, we found that the responses of birds change with increasing intensity. The analysis of the orientation of European robins under 502 nm turquoise light revealed two types of responses depending on light intensity: under a quantal flux of 8.10(15) quanta m(-2) s(-1), the birds showed normal migratory orientation in spring as well as in autumn, relying on their inclination compass. Under brighter light of 54.10(15) quanta m(-2) s(-1), however, they showed a "fixed" tendency toward north that did not undergo the seasonal change and proved to be based on magnetic polarity, not involving the inclination compass. When birds were exposed to a weak oscillating field, which specifically interferes with radical pair processes, the inclination compass response was disrupted, whereas the response to magnetic polarity remained unaffected. These findings indicate that the normal inclination compass used for migratory orientation is based on a radical-pair mechanism, whereas the fixed direction represents a novel type of light-dependent orientation based on a mechanism of a different nature.

The sea-finding behavior of hatchling olive ridley sea turtles, Lepidochelys olivacea, at the beach of San Miguel (Costa Rica).

Newly hatched olive ridley sea turtles (Lepidochelys olivacea) were tested for their directional preferences in a sand-filled circular arena in total darkness. Hatchlings that had crawled about 5 m on the beach, toward the sea preferred the southwesterly direction that would have brought them to the water line, whereas hatchlings that had been denied this experience headed eastward, a direction of unclear origin. These data suggest that a short crawl across the natural beach can set the direction in which the young turtles subsequently move. The crawling experience was sufficient to acquire the compass course that they later follow, probably with the help of a magnetic compass, not only in the water, but already while still on land.

Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field.

The radical pair model of magnetoreception predicts that magnetic compass orientation can be disrupted by high frequency magnetic fields in the Megahertz range. European robins, Erithacus rubecula, were tested under monochromatic 565 nm green light in 1.315 MHz fields of 0.48 microT during spring and autumn migration, with 1.315 MHz being the frequency that matches the energetic splitting induced by the local geomagnetic field. The birds' responses depended on the alignment of the oscillating field with respect to the static geomagnetic field: when the 1.315 MHz field was aligned parallel with the field lines, birds significantly preferred northerly directions in spring and southerly directions in autumn. These preferences reflect normal migratory orientation, with the variance slightly increased compared to control tests in the geomagnetic field alone or to tests in a 7.0 MHz field. However, in the 1.315 MHz field aligned at a 24 degrees angle to the field lines, the birds were disoriented in both seasons, indicating that the high frequency field interfered with magnetoreception. These finding are in agreement with theoretical predictions and support the assumption of a radical-pair mechanism underlying the processes mediating magnetic compass information in birds.

Visual lateralization and homing in pigeons.

The aim of our study was to analyse the components of visual lateralization in pigeon homing, a large-scale spatial task. In a series of 13 releases, birds were tested as binocular controls or monocularly with the right or left-eye covered. Occlusion of either eye had a significant effect on initial orientation and homing performance. Vanishing bearings were deflected to the side of the open eye, vanishing intervals were longer, and homing speed was reduced. These parameters were affected to a different degree. Initial orientation was markedly lateralized, with birds using their right-eye deviating less from the mean of control birds and showing significantly less variance. One minute after release, the deviation and variance were similarly large in both monocular groups. However, while the right-eyed birds improved their performance until leaving the release site, the left-eyed birds failed to do so. Vanishing intervals were similar in both monocular groups, but homing speed was reduced to a lesser extent in pigeons using the right-eye. The degree of lateralization varied across different releases, but superiority of the right-eye/left hemisphere prevailed. Lateralization did not depend on familiarity with the release site. This suggests that the crucial processes involved the eyes, but did not depend on visual memory of landscape features at the release site. Results reveal, for the first time, asymmetries of directional orientation as an essential component of lateralized homing performance. As likely mechanisms we suggest hemispheric differences in magnetic compass orientation and in the adjustment to optic flow.

Light-dependent magnetoreception in birds: interaction of at least two different receptors.

Passerine migrants require light from the blue-green part of the spectrum for magnetic compass orientation; under yellow light, they are disoriented. European robins tested under a combination of yellow light and blue or green light showed a change in behavior, no longer preferring their seasonally appropriate migratory direction: in spring as well as in autumn, they preferred southerly headings under blue-and-yellow and northerly headings under green-and-yellow light. This clearly shows that yellow light is not neutral and suggests the involvement of at least two types of receptors in obtaining magnetic compass information, with the specific interaction of these receptors being rather complex.