Katrin Stapput

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.

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.

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.

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.

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...

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.