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.     

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/m², 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/m², robins showed an axial preference in the east–west axis, whereas silvereyes preferred an easterly direction. At 5.7 mW/m², 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.     

An evaluation of LSU rDNA D1-D2 sequences for their use in species identification

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 8·10¹⁵ 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 36·10¹⁵ 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 36·10¹⁵ quanta s^-1 m^-2 to 54 and 72·10¹⁵ 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.     

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.     

Magnetoreception

The vector of the geomagnetic field provides animals with directional information, while intensity and/or inclination provide them with positional information. For magnetoreception, two hypotheses are currently discussed: one proposing magnetite-based mechanisms, the other suggesting radical pair processes involving photopigments. Behavioral studies indicate that birds use both mechanisms: they responded to a short, strong magnetic pulse designed to change the magnetization of magnetite particles, while, at the same time, their orientation was found to be light-dependent and could be disrupted by high-frequency magnetic fields in the MHz range, which is diagnostic for radical pair processes. Details of these findings, together with electrophysiological and histological studies, suggest that, in birds, a radical pair mechanism located in the right eye provides directional information for a compass, while a magnetite-based mechanism located in the upper beak records magnetic intensity, thus providing positional information. The mechanisms of magnetoreception in other animals have not yet been analyzed in detail.     

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.     

Use of a light-dependent magnetic compass for y-axis orientation in European common frog (Rana temporaria) tadpoles

We provide evidence for the use of a magnetic compass for y-axis orientation (i.e., orientation along the shore-deep water axis) by tadpoles of the European common frog (Rana temporaria). Furthermore, our study provides evidence for a wavelength-dependent effect of light on magnetic compass orientation in amphibians. Tadpoles trained and then tested under full-spectrum light displayed magnetic compass orientation that coincided with the trained shore-deep water axes of their training tanks. Conversely, tadpoles trained under long-wavelength (≥500 nm) light and tested under full-spectrum light, and tadpoles trained under full-spectrum light and tested under long-wavelength (≥500 nm) light, exhibited a 90° shift in magnetic compass orientation relative to the trained y-axis direction. Our results are consistent with earlier studies showing that the observed 90° shift in the direction of magnetic compass orientation under long-wavelength (≥500 nm) light is due to a direct effect of light on the underlying magnetoreception mechanism. These findings also show that wavelength-dependent effects of light do not compromise the function of the magnetic compass under a wide range of natural lighting conditions, presumably due to a large asymmetry in the relatively sensitivity of antagonistic short- and long-wavelength inputs to the light-dependent magnetic compass.     

Development of lateralization of the magnetic compass in a migratory bird

The magnetic compass of a migratory bird, the European robin (Erithacus rubecula), was shown to be lateralized in favour of the right eye/left brain hemisphere. However, this seems to be a property of the avian magnetic compass that is not present from the beginning, but develops only as the birds grow older. During first migration in autumn, juvenile robins can orient by their magnetic compass with their right as well as with their left eye. In the following spring, however, the magnetic compass is already lateralized, but this lateralization is still flexible: it could be removed by covering the right eye for 6 h. During the following autumn migration, the lateralization becomes more strongly fixed, with a 6 h occlusion of the right eye no longer having an effect. This change from a bilateral to a lateralized magnetic compass appears to be a maturation process, the first such case known so far in birds. Because both eyes mediate identical information about the geomagnetic field, brain asymmetry for the magnetic compass could increase efficiency by setting the other hemisphere free for other processes.     

The effect of yellow and blue light on magnetic compass orientation in European robins, Erithacus rubecula

To analyze the wavelength dependency of magnetic compass orientation, European robins were tested during spring migration under light of various wavelengths. Under 565-nm green light (control) the birds showed excellent orientation in their migratory direction; a 120° deflection of magnetic North resulted in a corresponding shift in the birds' directional tendencies, indicating the use of the magnetic compass. Under 443-nm blue light, the robins were likewise well oriented. Under 590-nm yellow, however, oriented behavior was no longer observed, although the activity was at the same level as under blue and green light. The spectral range where magnetic orientation is possible thus differs from the range of vision, the former showing parallels to that of rhodopsin absorption. The interpretation of the abrupt change in behavior observed between 565 green to 590 yellow is unclear. There is no simple relationship between magnetoreception and the known color receptors of birds. Accepted: 17 December 1998     

Magnetoreception and its use in bird navigation

Recent advances have brought new insight into the physiological mechanisms that enable birds and other animals to use magnetic fields for orientation. Many birds seem to have two magnetodetection senses, one based on magnetite near the beak and one based on light-dependent radical-pair processes in the bird's eye(s). Among the most exciting recent results are: first, behavioural responses of birds experiencing oscillating magnetic fields. Second, the occurrence of putative magnetosensory molecules, the cryptochromes, in the eyes of migratory birds. Third, detection of a brain area that integrates specialised visual input at night in night-migratory songbirds. Fourth, a putative magnetosensory cluster of magnetite in the upper beak. These and other recent findings have important implications for magnetoreception; however, many crucial open questions remain.     

Migratory orientation of European Robins is affected by the wavelength of light as well as by a magnetic pulse

The object of this study was to test the alternative hypotheses of magnetoreception by photopigments and magnetoreception based on magnetite. Migratory European Robins, Erithacus rubecula, were tested under light of different wavelengths; after these tests, they were subjected to a brief, strong magnetic pulse designed to alter the magnetization of single domain magnetite. In control tests under white light, the birds preferred the normal, seasonally appropriate migratory direction. Under 571 nm green light, they continued to be well oriented in the migratory direction, whereas under 633 nm red light, their behaviour was not different from random. The magnetic pulse had a significant effect on migratory orientation, but the response varied between individuals: some showed a persistent directional shift, while others exhibited a change in scatter; one bird was seemingly unaffected.These findings indicate a light-dependent process and, at the same time, suggest an involvement of magnetizable material in migratory orientation. They are in agreement with the model of a light-dependent compass and a magnetite-based map, even if some questions concerning the effect of the pulse remain open.     

Avian magnetic compass: Its functional properties and physical basis

The avian magnetic compass was analyzed in bird species of three different orders - Passeriforms, Columbiforms and Galliforms - and in three different behavioral contexts, namely migratory orientation, homing and directional conditioning. The respective findings indicate similar functional properties: it is an inclination compass that works only within a functional window around the ambient magnetic field intensity, it tends to be lateralized in favor of the right eye, and it is wavelength-dependent, requiring light from the short-wavelength range of the spectrum. The underlying physical mechanisms have been identified as radical pair processes, spin-chemical reactions in specialized photopigments. The iron-based receptors in the upper beak do not seem to be involved. The existence of the same type of magnetic compass in only very distantly related bird species suggests that it may have been present already in the common ancestors of all modern birds, where it evolved as an all-purpose compass mechanism for orientation within the home range.     

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.     

鸟类利用地磁场定向的机制

地磁场和生物体问的相互作用关系是一个很有趣的未解之迷.虽然对地磁场的生物学作用至今还知之不多,为过近来有关鸟类利用地磁场信息定向的研究取得了较大的进展.很多鸟类能够对地磁场和外加磁场信息做出反应,这些反应可能通过磁场一生物化学过程介导.对此,目前有两种被广为接受的解释,一种认为在鸟喙上方存在一个磁场信息感受器,另一种认为通过视觉成像系统感受磁场信息.另外,最近研究发现磁场信息的感知分析功能有明显的单侧优势特征.虽然目前有关鸟类利用磁场信息定向的研究取得了很多进展,但是要想解释并利用鸟类的磁场定向功能还有很多工作要做.本文结合最近的研究发现对这一有趣的问题进行了综述.     

Bats use magnetite to detect the earth's magnetic field

While the role of magnetic cues for compass orientation has been confirmed in numerous animals, the mechanism of detection is still debated. Two hypotheses have been proposed, one based on a light dependent mechanism, apparently used by birds and another based on a "compass organelle" containing the iron oxide particles magnetite (Fe(3)O(4)). Bats have recently been shown to use magnetic cues for compass orientation but the method by which they detect the Earth's magnetic field remains unknown. Here we use the classic "Kalmijn-Blakemore" pulse re-magnetization experiment, whereby the polarity of cellular magnetite is reversed. The results demonstrate that the big brown bat Eptesicus fuscus uses single domain magnetite to detect the Earths magnetic field and the response indicates a polarity based receptor. Polarity detection is a prerequisite for the use of magnetite as a compass and suggests that big brown bats use magnetite to detect the magnetic field as a compass. Our results indicate the possibility that sensory cells in bats contain freely rotating magnetite particles, which appears not to be the case in birds. It is crucial that the ultrastructure of the magnetite containing magnetoreceptors is described for our understanding of magnetoreception in animals.     

Magnetic orientation in birds: non-compass responses under monochromatic light of increased intensity

Migratory Australian silvereyes (Zosterops lateralis) were tested under monochromatic light at wavelengths of 424 nm blue and 565 nm green. At a low light level of 7 x 10(15) quanta m(-2) s(-1) in the local geomagnetic field, the birds preferred their seasonally appropriate southern migratory direction under both wavelengths. Their reversal of headings when the vertical component of the magnetic field was inverted indicated normal use of the avian inclination compass. A higher light intensity of 43 x 10(15) quanta m(-2) s(-1), however, caused a fundamental change in behaviour: under bright blue, the silvereyes showed an axial tendency along the east-west axis; under bright green, they showed a unimodal preference of a west-northwesterly direction that followed a shift in magnetic north, but was not reversed by inverting the vertical component of the magnetic field. Hence it is not based on the inclination compass. The change in behaviour at higher light intensities suggests a complex interaction between at least two receptors. The polar nature of the response under bright green cannot be explained by the current models of light-dependent magnetoreception and will lead to new considerations on these receptive processes.     

Light-Dependent Shift in Bullfrog Tadpole Magnetic Compass Orientation: Evidence for a Common Magnetoreception Mechanism in Anuran and Urodele Amphibians

Previous studies have demonstrated the presence of a light‐dependent magnetic compass in a urodele amphibian, the eastern red‐spotted newt Notophthalmus viridescens, mediated by extraocular photoreceptors located in or near the pineal organ. Newts tested under long‐wavelength (≥500 nm) light exhibited a 90° shift in the direction of orientation relative to newts tested under full spectrum (white) or short‐wavelength light. Here we report that bullfrog tadpoles Rana catesbeiana (an anuran amphibian) exhibit a 90° shift in the direction of magnetic compass orientation under long‐wavelength (≥500 nm) light similar to that observed in newts, suggesting that a common light‐dependent mechanism mediates these responses. These findings suggest that a light‐dependent magnetic compass may have been the ancestral state in this group of vertebrates.     

The puzzle of magnetic resonance effect on the magnetic compass of migratory birds

Experiments on the effect of radio‐frequency (RF) magnetic fields on the magnetic compass orientation of migratory birds are analyzed using the theory of magnetic resonance. The results of these experiments were earlier interpreted within the radical‐pair model of magnetoreception. However, the consistent analysis shows that the amplitudes of the RF fields used are far too small to noticeably influence electron spins in organic radicals. Other possible agents that could mediate the birds' response to the RF fields are discussed, but apparently no known physical system can be responsible for this effect. Bioelectromagnetics 30:402–410, 2009. © 2009 Wiley‐Liss, Inc.     

Behavioural and physiological mechanisms of polarized light sensitivity in birds

Polarized light (PL) sensitivity is relatively well studied in a large number of invertebrates and some fish species, but in most other vertebrate classes, including birds, the behavioural and physiological mechanism of PL sensitivity remains one of the big mysteries in sensory biology. Many organisms use the skylight polarization pattern as part of a sun compass for orientation, navigation and in spatial orientation tasks. In birds, the available evidence for an involvement of the skylight polarization pattern in sun-compass orientation is very weak. Instead, cue-conflict and cue-calibration experiments have shown that the skylight polarization pattern near the horizon at sunrise and sunset provides birds with a seasonally and latitudinally independent compass calibration reference. Despite convincing evidence that birds use PL cues for orientation, direct experimental evidence for PL sensitivity is still lacking. Avian double cones have been proposed as putative PL receptors, but detailed anatomical and physiological evidence will be needed to conclusively describe the avian PL receptor. Intriguing parallels between the functional and physiological properties of PL reception and light-dependent magnetoreception could point to a common receptor system.     

Light-dependent orientation responses in animals can be explained by a model of compass cue integration

The magnetic compass sense of animals is currently thought to be based on light-dependent processes like the proposed radical pair mechanism. In accordance, many animals show orientation responses that depend on light. However, the orientation responses depend on the wavelength and irradiance of monochromatic light in rather complex ways that cannot be explained directly by the radical pair mechanism. Here, a radically different model is presented that can explain a vast majority of the complex observed light-dependent responses. The model put forward an integration process consisting of simple lateral inhibition between a normal functioning, light-independent magnetic compass (e.g. magnetite based) and a vision based skylight color gradient compass that misperceives compass cues in monochromatic light. Integration of the misperceived color compass cue and the normal magnetic compass not only explains most of the categorically different light-dependent orientation responses, but also shows a surprisingly good fit to how well the animals are oriented (r-values) under light of different wavelength and irradiance. The model parsimoniously suggests the existence of a single magnetic sense in birds (probably based on magnetic crystals).