A model for photoreceptor-based magnetoreception in birds

A large variety of animals has the ability to sense the geomagnetic field and utilize it as a source of directional (compass) information. It is not known by which biophysical mechanism this magnetoreception is achieved. We investigate the possibility that magnetoreception involves radical-pair processes that are governed by anisotropic hyperfine coupling between (unpaired) electron and nuclear spins. We will show theoretically that fields of geomagnetic field strength and weaker can produce significantly different reaction yields for different alignments of the radical pairs with the magnetic field. As a model for a magnetic sensory organ we propose a system of radical pairs being 1) orientationally ordered in a molecular substrate and 2) exhibiting changes in the reaction yields that affect the visual transduction pathway. We evaluate three-dimensional visual modulation patterns that can arise from the influence of the geomagnetic field on radical-pair systems. The variations of these patterns with orientation and field strength can furnish the magnetic compass ability of birds with the same characteristics as observed in behavioral experiments. We propose that the recently discovered photoreceptor cryptochrome is part of the magnetoreception system and suggest further studies to prove or disprove this hypothesis.     

Compass Orientation During Dispersal of Freshwater Hatchling Snapping Turtles (Chelydra serpentina) and Blanding's Turtles (Emydoidea blandingii)

Freshwater turtle hatchlings primarily use visual cues for orientation while dispersing from nests; however, hatchlings rapidly develop a relationship between a sun or geomagnetic compass and a dispersal target that allows them to maintain an established direction of movement when target habitats are not visible. We examined dispersal patterns of hatchling snapping turtles (Chelydra serpentina) and Blanding's turtles (Emydoidea blandingii) dispersing in large arenas in a mowed field and in dense corn. The dispersal of three categories of hatchlings were examined: (1) naïve individuals (no previous dispersal experience), (2) arena‐experienced (limited dispersal experience in arenas in natural habitat), and (3) natural‐experienced hatchling Blanding's turtles (captured after extensive experience dispersing W in natural habitats toward wetlands). Experienced hatchlings were assigned to treatments consisting of having a magnet or a non‐magnetic aluminum sham or nothing glued to their anterior carapace before release in the corn arena. Dispersal patterns of naïve hatchlings of both species were strongly directional in the field arena with visible target horizons and primarily random in the corn arena where typical target horizons were blocked. When released in corn, dispersal patterns were similar for arena‐experienced hatchlings with magnets or shams attached and differed from their prior dispersal headings in the field arena as naïve hatchlings. Natural‐experienced hatchling Blanding's turtles with and without magnets were able to accurately maintain their prior headings to the WNW while dispersing in the field or corn arenas (i.e., the presence of a magnet did not disrupt their ability to maintain their prior heading). Based on the assumption that no other type of compass exists in hatchlings, we conclude that they were not using a geomagnetic compass, but by default were using sun compass orientation to maintain dispersal headings in dense corn where no typical target habitats were visible.     

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.     

Involvement of the sun and the magnetic compass of domestic fowl in its spatial orientation

Domestic chicks are able to find a food goal at different times of day, with the sun as the only consistent visual cue. This suggests that domestic chickens may use the sun as a time-compensated compass, rather than as a beacon. An alternative explanation is that the birds might use the earth's magnetic field. In this study, we investigated the role of the sun compass in a spatial orientation task using a clock-shift procedure. Furthermore, we investigated whether domestic chickens use magnetic compass information when tested under sunny conditions.Ten ISA Brown chicks were housed in outdoor pens. A separate test arena comprised an open-topped, opaque-sided, wooden octagonal maze. Eight goal boxes with food pots were attached one to each of the arena sides. A barrier inside each goal box prevented the birds from seeing the food pot before entering. After habituation, we tested in five daily 5-min trials whether chicks were able to find food in an systematically allocated goal direction. We controlled for the use of olfactory cues and intra-maze cues. No external landmarks were visible. All tests were done under sunny conditions. Circular statistics showed that nine chicks significantly oriented goalwards using the sun as the only consistent visual cue during directional testing. Next, these nine chicks were subjected to a clock-shift procedure to test for the role of sun-compass information. The chicks were housed indoors for 6 days on a light-schedule that was 6 h ahead of the natural light–dark schedule. After clock-shifting, the birds were tested again and all birds except one were disrupted in their goalward orientation. For the second experiment, six birds were re-trained and fitted with a tiny, powerful magnet on the head to disrupt their magnetic sense. The magnets did not affect the chicks’ goalward orientation.In conclusion, although the strongest prediction of the sun-compass hypothesis (significant re-orientation after clock-shifting) was neither confirmed nor refuted, our results suggest that domestic chicks use the sun as a compass rather than as a beacon. These findings suggest that hens housed indoors in large non-cage systems may experience difficulties in orientation if adequate alternative cues are unavailable. Further research should elucidate how hens kept in non-cage systems orient in space in relation to available resources.     

You Can Get There from Here: Responses to Simulated Magnetic Equator Crossing by the Bobolink (Dolichonyx oryzivorus)

The avian magnetic compass works as an inclination compass. Instead of using the polarity of the magnetic field to determine direction, birds use the inclination of the dip angle. Consequently, transequatorial migrants have to reverse their response to the magnetic compass after crossing the magnetic equator. When confronted with an artificial magnetic field that reverses the vertical component of the magnetic field, migrants such as the bobolink reverse their headings relative to magnetic north even in the presence of visual cues such as stellar patterns. Bobolinks, which breed in temperate North America and winter in temperate South America, were tested in a planetarium under fixed star patterns in a series of magnetic fields incremented each night from the natural field in the northern hemisphere through an artificial horizontal field to an artificial southern hemisphere magnetic field. The birds maintained a constant heading throughout the experiment and did not reverse direction after the simulated crossing of the magnetic equator as previous experiments predicted. In nature, this response would have meant continuation of their migration flight across the equator and into the opposite hemisphere. The switch from “equatorward” orientation to “poleward” orientation is probably triggered by experience with a horizontal magnetic field and/or visual cues. The ability to maintain an accurate heading while crossing the magnetic equator may be based on the use of visual cues such as the stars.     

Cryptochrome Mediates Light-Dependent Magnetosensitivity of Drosophila's Circadian Clock

Since 1960, magnetic fields have been discussed as Zeitgebers for circadian clocks, but the mechanism by which clocks perceive and process magnetic information has remained unknown. Recently, the radical-pair model involving light-activated photoreceptors as magnetic field sensors has gained considerable support, and the blue-light photoreceptor cryptochrome (CRY) has been proposed as a suitable molecule to mediate such magnetosensitivity. Since CRY is expressed in the circadian clock neurons and acts as a critical photoreceptor of Drosophila's clock, we aimed to test the role of CRY in magnetosensitivity of the circadian clock. In response to light, CRY causes slowing of the clock, ultimately leading to arrhythmic behavior. We expected that in the presence of applied magnetic fields, the impact of CRY on clock rhythmicity should be altered. Furthermore, according to the radical-pair hypothesis this response should be dependent on wavelength and on the field strength applied. We tested the effect of applied static magnetic fields on the circadian clock and found that flies exposed to these fields indeed showed enhanced slowing of clock rhythms. This effect was maximal at 300 μT, and reduced at both higher and lower field strengths. Clock response to magnetic fields was present in blue light, but absent under red-light illumination, which does not activate CRY. Furthermore, cry^b and cry^OUT mutants did not show any response, and flies overexpressing CRY in the clock neurons exhibited an enhanced response to the field. We conclude that Drosophila's circadian clock is sensitive to magnetic fields and that this sensitivity depends on light activation of CRY and on the applied field strength, consistent with the radical pair mechanism. CRY is widespread throughout biological systems and has been suggested as receptor for magnetic compass orientation in migratory birds. The present data establish the circadian clock of Drosophila as a model system for CRY-dependent magnetic sensitivity. Furthermore, given that CRY occurs in multiple tissues of Drosophila, including those potentially implicated in fly orientation, future studies may yield insights that could be applicable to the magnetic compass of migratory birds and even to potential magnetic field effects in humans.     

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.     

Avian orientation at steep angles of inclination: experiments with migratory white-crowned sparrows at the magnetic North Pole

The Earth's magnetic field and celestial cues provide animals with compass information during migration. Inherited magnetic compass courses are selected based on the angle of inclination, making it difficult to orient in the near vertical fields found at high geomagnetic latitudes. Orientation cage experiments were performed at different sites in high Arctic Canada with adult and young white-crowned sparrows (Zonotrichia leucophrys gambelii) in order to investigate birds' ability to use the Earth's magnetic field and celestial cues for orientation in naturally very steep magnetic fields at and close to the magnetic North Pole. Experiments were performed during the natural period of migration at night in the local geomagnetic field under natural clear skies and under simulated total overcast conditions. The experimental birds failed to select a meaningful magnetic compass course under overcast conditions at the magnetic North Pole, but could do so in geomagnetic fields deviating less than 3 degrees from the vertical. Migratory orientation was successful at all sites when celestial cues were available.     

Quantitative Modeling and Optimization of Magnetic Tweezers

Magnetic tweezers are a powerful tool to manipulate single DNA or RNA molecules and to study nucleic acid-protein interactions in real time. Here, we have modeled the magnetic fields of permanent magnets in magnetic tweezers and computed the forces exerted on superparamagnetic beads from first principles. For simple, symmetric geometries the magnetic fields can be calculated semianalytically using the Biot-Savart law. For complicated geometries and in the presence of an iron yoke, we employ a finite-element three-dimensional PDE solver to numerically solve the magnetostatic problem. The theoretical predictions are in quantitative agreement with direct Hall-probe measurements of the magnetic field and with measurements of the force exerted on DNA-tethered beads. Using these predictive theories, we systematically explore the effects of magnet alignment, magnet spacing, magnet size, and of adding an iron yoke to the magnets on the forces that can be exerted on tethered particles. We find that the optimal configuration for maximal stretching forces is a vertically aligned pair of magnets, with a minimal gap between the magnets and minimal flow cell thickness. Following these principles, we present a configuration that allows one to apply ≥40 pN stretching forces on ≈1-μm tethered beads.     

Magnetic compass orientation in the Eastern red-spotted newt (Notophthalmus viridescens)

Summary Laboratory tests were carried out to examine the orientation behavior of adult Eastern red-spotted newts (Notophthalmus viridescens) to earth-strength magnetic fields. Groups of 30 to 40 newts were housed in water-filled, all-glass aquaria with an artificial shoreline at one end. The aquaria were located in a greenhouse or outdoors adjacent to the laboratory building, and aligned on either the magnetic north-south or east-west axis. Tests were carried out in an enclosed indoor arena. Newts were tested in four horizontal alignments of the magnetic field: the ambient magnetic field (magnetic north at North) and three altered fields (magnetic north rotated to East, South or West). Data were analyzed after pooling the magnetic bearings from all four conditions in such a way as to retain the component of the newts' orientation that was a consistent response to the magnetic field. Elevation of training tank water temperature was used to increase the newts' motivation to orient in the direction of shore. Newts exposed to a training tank water temperature of 33–34 °C just prior to testing exhibited consistent unimodal magnetic compass orientation. The direction of orientation was altered predictably by changing training tank alignment and location relative to the laboratory building. The results provide the first evidence of a strong, replicable magnetic compass response in a terrestrial vertebrate under controlled laboratory conditions. Further, the present study demonstrates that the Eastern newt is able to learn a directional response relative to the earth's magnetic field.     

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.     

Optimization of static magnetic field parameters improves analgesic effect in mice

The present study deals with the analgesic effect induced by static magnetic fields (SMF) in mice exposed to the field with their whole body. It discusses how the effect depends on the distribution of the magnetic field, that is, on the specification and arrangement of the applied individual permanent magnets. A critical analysis of different magnet arrangements is given. As a result the authors propose a magnet arrangement recipe that achieves an analgesic effect of over 80% in the writhing test. This is a widely accepted screening method for animal pain and predictor of human experimental results. As a non-drug, non-invasive, non-contact, non-pain, non-addictive method for analgesia with immediate and long-lasting effect based on the stimulus of the endogenous opioid network, the SMF treatment may attract the attention of medical doctors, nurses, magnet therapists, veterinarians, physiotherapists, masseurs, and fitness trainers among others.     

The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds

Recent advances have brought much new insight into the physiological mechanisms and required characteristics of the sensory molecules that enable birds to use magnetic fields for orientation. European robins almost certainly have two magnetodetection senses, one associated with the ophthalmic branch of the trigeminal nerve, and one based on light-dependent radical-pair processes in both eyes. The first brain areas processing magnetic information from each of these two senses have been identified. It has been experimentally verified that Earth-strength magnetic fields can affect photo-induced chemical reactions and that these reactions can respond to magnetic field direction. Diagnostic behavioural experiments have provided clues to identify putative magnetoreceptive molecules in the retina. We discuss the implications of these and other recent findings and outline crucial open questions with an emphasis on the light-dependent mechanism.     

The Magnetic Field as a Reference System for Genetically Encoded Migratory Direction in Pied Flycatchers (Ficedula hypoleuca Pallas)

To see whether the migratory orientation of pied flycatchers (Ficedula hypoleuca Pallas) is genetically encoded with respect to the earth magnetic field a group of young birds was hand-raised. They were thus prevented from ever experiencing the sky. The birds were tested in autumn 1980 and 1981 in the local geomagnetic field (Fig. 1) and in three artificial fields (Fig. 2a-c). The results show that their magnetic compass matures independent of any experience with the sky and contains sufficient information for the birds to orient toward their migratory direction.     

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.     

Use of an Inclination Compass during Migratory Orientation by the Bobolink (Dolichonyx oryzivorus)

Adult bobolinks were tested in a planetarium under patterns of nonrotating artificial stars to determine the influence of natural and modified magnetic fields on their migratory orientation. The modified magnetic field was of the same total intensity as the natural field, but the vertical vector was reversed, causing the resulting total vector to point up and north (compared to the natural northern hemisphere vector pointing down and north). When exposed to the artificial magnetic field, the birds reversed their preferred headings relative to the stellar and geographic references. This response is consistent with the use of an inclination compass. Although 60 % of the individuals reversed their headings the first night, some individuals took up to 5 nights (mean = 2.1 nights).     

Magnetic field effects in Arabidopsis thaliana cryptochrome-1

The ability of some animals, most notably migratory birds, to sense magnetic fields is still poorly understood. It has been suggested that this "magnetic sense" may be mediated by the blue light receptor protein cryptochrome, which is known to be localized in the retinas of migratory birds. Cryptochromes are a class of photoreceptor signaling proteins that are found in a wide variety of organisms and that primarily perform regulatory functions, such as the entrainment of circadian rhythm in mammals and the inhibition of hypocotyl growth in plants. Recent experiments have shown that the activity of cryptochrome-1 in Arabidopsis thaliana is enhanced by the presence of a weak external magnetic field, confirming the ability of cryptochrome to mediate magnetic field responses. Cryptochrome's signaling is tied to the photoreduction of an internally bound chromophore, flavin adenine dinucleotide. The spin chemistry of this photoreduction process, which involves electron transfer from a chain of three tryptophans, can be modulated by the presence of a magnetic field in an effect known as the radical-pair mechanism. Here we present and analyze a model of the flavin-adenine-dinucleotide-tryptophan chain system that incorporates realistic hyperfine coupling constants and reaction rate constants. Our calculations show that the radical-pair mechanism in cryptochrome can produce an increase in the protein's signaling activity of approximately 10% for magnetic fields on the order of 5 G, which is consistent with experimental results. These calculations, in view of the similarity between bird and plant cryptochromes, provide further support for a cryptochrome-based model of avian magnetoreception.     

Bats respond to polarity of a magnetic field

Bats have been shown to use information from the Earth's magnetic field during orientation. However, the mechanism underlying this ability remains unknown. In this study we investigated whether bats possess a polarity- or inclination-based compass that could be used in orientation. We monitored the hanging position of adult Nyctalus plancyi in the laboratory in the presence of an induced magnetic field of twice Earth-strength. When under the influence of a normally aligned induced field the bats showed a significant preference for hanging at the northern end of their roosting basket. When the vertical component of the field was reversed, the bats remained at the northern end of the basket. However, when the horizontal component of the field was reversed, the bats changed their positions and hung at the southern end of the basket. Based on these results, we conclude that N. plancyi, unlike all other non-mammalian vertebrates tested to date, uses a polarity-based compass during orientation in the roost, and that the same compass is also likely to underlie bats' long-distance navigation abilities.     

Effects of non-uniform static magnetic fields on the rate of myosin phosphorylation

The effect on myosin phosphorylation from exposure to a magnetic field generated by an array of four permanent magnets was investigated. Two lateral positions in the non-uniform field over the array were explored, each at four vertical distances over the surface of the device. The rate of myosin phosphorylation was found to depend on the position laterally over the array as well as the distance from the device surface. The square magnet array was comprised of axially magnetized, cylindrical NdFeB permanent magnets arranged with poles of alternating polarity in a plane (MagnaBloc trade mark therapeutic device). Detailed dosimetry of the magnet array was compiled: the magnetic flux density averaged over the exposure volume spanned the range 0.7-86 mT for the eight different exposure positions. The corresponding range for the absolute field gradient was 0.4-20 T/m. Comparing the dosimetry to the experimental outcome, our results imply that magnetic field amplitude alone is not sufficient to describe the influence of the field in this preparation.