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.     

Biogenic magnetite as a basis for magnetic field detection in animals

Bacteria, sharks, honey bees, and homing pigeons as well as other organisms seem to detect the direction of the earth's magnetic field. Indirect but reproducible evidence suggests that the bees and birds can also respond to very minute changes in its intensity. The mechanisms behind this sensitivity are not known. Naturally magnetic, biologically precipitated magnetite (Fe₃O₄) has been found in chitons, magnetotactic bacteria, honey bees, homing pigeons, and dolphins. Its mineralization in localized areas may be associated with the ability of these animals to respond to the direction and intensity of the earth's magnetic field. The presence of large numbers (～10⁸) of superparamagnetic magnetite crystals in honey bees and similar numbers of single-domain magnetite grains in pigeons suggests that there may be at least two basic types of ferrimagnetic magnetoreceptive organelles. Theoretical calculations show that ferrimagnetic organs using either type of grain when integrated by the nervous system are capable of accounting for even the most extreme magnetic field sensitivities reported. Indirect evidence suggests that organic magnetite may be a common biological component, and may account for the results of numerous high field and electromagnetic experiments on animals.     

Spontaneous preferences for magnetic compass direction in the American red-spotted newt, <Emphasis Type="Italic">Notophthalmus viridescens</Emphasis> (Salamandridae,Urodela)

In addition to other sensory modalities, migratory vertebrates are able to use the earths’ magnetic field for orientation and navigation. The magnetic cue may also serve as a reference for other orientation mechanisms. In this study, significant evidence is shown that, even in darkness, newts (Notophthalmus viridescens, Salamandridae) spontaneously align according to the natural or to the deviated earth’s magnetic field lines, thereby demonstrating a magnetic compass sensitivity. All newts preferred compass directions close to east or west or chose the E/W axially and hence sought to maintain a specific angle or axis relative to the magnetic field vector. Such an active alignment is considered an essential precondition for magnetic orientation. When the horizontal magnetic vector was experimentally compensated, animals became disoriented. We infer that the animals have either learned the preferred magnetic direction/axis individually or that these choices are innate and could even be seasonally different as in migrating birds. It is still an unanswered question as to how and where the physical and physiological mechanisms of magnetic transduction and reception take place. The visual system and other light-dependent (radical pairs) mechanisms alone are often claimed to be in function, but this must now be reconsidered given the results from animals when deprived of light. The results may therefore point to putative receptor mechanisms involving magnetite elements in specialized magneto-receptors.     

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).     

Magnetic and other non-visual orientation mechanisms in some cave and surface urodeles

Animals adapted to light-deprived habitats might have improved non-visual sensory systems. Specimens of several cave-dwelling species of urodeles spontaneously and persistently align to natural or artificially-modified permanent magnetic fields. Video observations under dim infrared illumination revealed an obvious individual preference for one particular magnetic direction in every animal tested. Therefore, animals changed alignments predictably when the horizontal magnetic field vector (compass direction) was artificially reversed or deviated. When the vertical vector was compensated, individuals aligned axially. With the vertical vector reversed (inclination upward), either axial alignment was still typical, or the individuals behaved as with the horizontal vector reversed. However, reactions as to the natural field occurred as well. The findings suggest a receptor mechanism that needs both horizontal and vertical magnetic cues, but it is still an open question how and where the physical and physiological mechanisms of magnetic transduction and reception are realized. The visual system is likely not necessary because Proteus is ontogenetically deprived of eyesight, and the other species were blindfolded due to the faint infrared illumination. The results therefore tend to favor those putative receptor mechanisms, assumed to work by means of magnetite nano-elements. In sum, the ability to align within the geomagnetic field may be considered a prerequisite for magnetic orientation and is, among other sensory improvements, judged to be highly relevant as an important sensorial and ecological adaptation to light-deprived habitats.     

Magnetic Compass Orientation in Larval Iberian Green Frogs, Pelophylax Perezi

Experiments were carried out to investigate whether Iberian green frog tadpoles Pelophylax perezi (formerly Rana perezi) are able of using the geomagnetic field for y‐axis orientation (i.e. orientation toward and away from shore). Tadpoles were trained outdoor for 5 d, in two different training configurations: (i) a training tank aligned along the magnetic north–south axis, with shore facing south, and (ii) a training tank aligned along the magnetic east–west axis, with shore located east, and similar to the shore–deep water axis (‘y‐axis’) found in their home stream, which flows from south to north. After training, tadpoles were individually tested for magnetic orientation in a water‐filled circular outdoor arena surrounded by a pair of orthogonally aligned cube‐surface‐coils used to alter the alignment of the earth's magnetic field. Tadpoles held in the east–west training tank oriented towards shore, indicating that they were able to distinguish between the shoreward and waterward direction along the y‐axis. Tadpoles trained in the tank that was aligned along the north–south axis showed bimodal magnetic compass orientation along the shore–deep water magnetic axis. These findings provide evidence for the use of magnetic compass cues for y‐axis orientation by P. perezi tadpoles.     

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.     

Bird navigation: what type of information does the magnetite-based receptor provide?

Previous experiments have shown that a short, strong magnetic pulse caused migratory birds to change their headings from their normal migratory direction to an easterly direction in both spring and autumn. In order to analyse the nature of this pulse effect, we subjected migratory Australian silvereyes, Zosterops lateralis, to a magnetic pulse and tested their subsequent response under different magnetic conditions. In the local geomagnetic field, the birds preferred easterly headings as before, and when the horizontal component of the magnetic field was shifted 90 degrees anticlockwise, they altered their headings accordingly northwards. In a field with the vertical component inverted, the birds reversed their headings to westwards, indicating that their directional orientation was controlled by the normal inclination compass. These findings show that although the pulse strongly affects the magnetite particles, it leaves the functional mechanism of the magnetic compass intact. Thus, magnetite-based receptors seem to mediate magnetic 'map'-information used to determine position, and when affected by a pulse, they provide birds with false positional information that causes them to change their course.     

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.     

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.     

Target-directed Orientation in Displaced Honeybees

Under sunny weather conditions, displaced honeybees (Apis mellifera) usually fly into the celestial compass direction and thus may be misled from their goal, or they are disorientated. Under cloudy conditions, they may determine the celestial compass direction from prominent landmarks. They may also fly directly toward their goal from a release site. In two experiments, we investigated the orientation of displaced bees when a landmark (target) was close to the goal under different weather conditions. It is shown that in sunny conditions, the celestial compass will override target orientation under most conditions. Under 100% cloud cover, the celestial compass direction retrieved from landmarks modulates target-orientated behaviour but is not by itself a primary orientation factor. The bees will fly toward a previously encountered landmark that signals the target, and in case of several similar landmarks which are visible to the bees, they will choose the one in the direction nearest the celestial compass direction. The results indicate that honeybee orientation is the result of a set of context-specific interdependent orientation mechanisms.     

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.     

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.     

Behavioural evidence that magnetic field effects in the land snail,Cepaea nemoralis,might not depend on magnetite or induced electric currents

Although extremely low frequency (ELF) magnetic fields (<300 Hz) appear to exert a variety of biological effects, the magnetic field sensing/transduction mechanism(s) remains to be established. Here, using the inhibitory effects of magnetic fields on endogenous opioid peptide-mediated “analgaesic” response of the land snail. Cepaea nemoralis, we addressed the mechanism(s) of action of ELF magnetic fields. Indirect mechanisms involving both induced electric fields and direct magnetic field detection mechanisms (e.g., magnetite, parametric resonance) were evaluated. Snails were exposed to a static magnetic field (B_DC=78±1 μT) and to a 60 Hz magnetic field (B_AC=299±1 μT peak) with the angle between the static and 60 Hz magnetic fields varied in eight steps between 0° and 90°. At 0° and 90°, the magnetic field reduced opioid-induced analgaesia by approximately 20%, and this inhibition was increased to a maximum of 50% when the angle was between 50° and 70°. Because B_AC was fixed in amplitude, direction, and frequency, any induced electric currents would be constant independent of the B_AC/B_DC angle. Also, an energy transduction mechanism involving magnetite should show greatest sensitivity at 90°. Therefore, the energy transduction mechanism probably does not involve induced electric currents or magnetite. Rather, our results suggest a direct magnetic field detection mechanism consistent with the parametric resonance model proposed by Lednev. © 1996 Wiley-Liss, Inc.     

Polarization Orientation,Piezoelectricity, and Energy Harvesting Performance of Ferroelectric PVDF‐TrFE Nanotubes Synthesized by Nanoconfinement

1D nanostructures of soft ferroelectric materials exert promising potential in the fields of energy harvesting and flexible and printed nanoelectronics. Here, improved piezoelectric properties, energy‐harvesting performance, lower coercive fields, and the polarization orientation of poly(vinylidene fluoride–trifluoroethylene) (PVDF‐TrFE) nanotubes synthesized with nanoconfinement effect are reported. X‐ray diffraction (XRD) patterns of the nanotubes show the peak corresponding to the planes of (110)/(200), which is a signature of ferroelectric beta phase formation. Piezoforce spectroscopy measurements on the free‐standing horizontal nanotubes bundles reveal that the effective polarization direction is oriented at an inclination to the long axis of the nanotubes. The nanotubes exhibit a coercive field of 18.6 MV m^?1 along the long axis and 40 MV m^?1 (13.2 MV m^?1 considering the air gap) in a direction perpendicular to the long axis, which is lower than the film counterpart of 50 MV m^?1. The poled 200 nm nanotubes, with 40% reduction in poling field, give larger piezoelectric d₃₃ coefficient values of 44 pm V^?1, compared to poled films (≈20 pm V^?1). The ferroelectric nanotubes deliver superior energy harvesting performance with an output voltage of ≈4.8 V and power of 2.2 μW cm^?2, under a dynamic compression pressure of 0.075 MPa at 1 Hz.     

Rapid Learning of Magnetic Compass Direction by C57BL/6 Mice in a 4-Armed ‘Plus’ Water Maze

Magnetoreception has been demonstrated in all five vertebrate classes. In rodents, nest building experiments have shown the use of magnetic cues by two families of molerats, Siberian hamsters and C57BL/6 mice. However, assays widely used to study rodent spatial cognition (e.g. water maze, radial arm maze) have failed to provide evidence for the use of magnetic cues. Here we show that C57BL/6 mice can learn the magnetic direction of a submerged platform in a 4-armed (plus) water maze. Naïve mice were given two brief training trials. In each trial, a mouse was confined to one arm of the maze with the submerged platform at the outer end in a predetermined alignment relative to magnetic north. Between trials, the training arm and magnetic field were rotated by 180^° so that the mouse had to swim in the same magnetic direction to reach the submerged platform. The directional preference of each mouse was tested once in one of four magnetic field alignments by releasing it at the center of the maze with access to all four arms. Equal numbers of responses were obtained from mice tested in the four symmetrical magnetic field alignments. Findings show that two training trials are sufficient for mice to learn the magnetic direction of the submerged platform in a plus water maze. The success of these experiments may be explained by: (1) absence of alternative directional cues (2), rotation of magnetic field alignment, and (3) electromagnetic shielding to minimize radio frequency interference that has been shown to interfere with magnetic compass orientation of birds. These findings confirm that mice have a well-developed magnetic compass, and give further impetus to the question of whether epigeic rodents (e.g., mice and rats) have a photoreceptor-based magnetic compass similar to that found in amphibians and migratory birds.     

Integration of polarization and chromatic cues in the insect sky compass

Animals relying on a celestial compass for spatial orientation may use the position of the sun, the chromatic or intensity gradient of the sky, the polarization pattern of the sky, or a combination of these cues as compass signals. Behavioral experiments in bees and ants, indeed, showed that direct sunlight and sky polarization play a role in sky compass orientation, but the relative importance of these cues are species-specific. Intracellular recordings from polarization-sensitive interneurons in the desert locust and monarch butterfly suggest that inputs from different eye regions, including polarized-light input through the dorsal rim area of the eye and chromatic/intensity gradient input from the main eye, are combined at the level of the medulla to create a robust compass signal. Conflicting input from the polarization and chromatic/intensity channel, resulting from eccentric receptive fields, is eliminated at the level of the anterior optic tubercle and central complex through internal compensation for changing solar elevations, which requires input from a circadian clock. Across several species, the central complex likely serves as an internal sky compass, combining E-vector information with other celestial cues. Descending neurons, likewise, respond both to zenithal polarization and to unpolarized cues in an azimuth-dependent way.     

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.     

Innate preference for magnetic compass direction in the Alpine newt, <Emphasis Type="Italic">Triturus alpestris</Emphasis> (Salamandridae,Urodela)?

Magnetic compass orientation was first discovered for migrating/homing birds in which all individuals of a population or species prefer a predictable magnetic direction during a particular migratory situation. If all other sensory cues are absent, the Earth’s magnetic field may serve as a reference for other orientation mechanisms. It will be demonstrated that alpine newts (Triturus alpestris, Salamandridae) spontaneously align according to the natural or the deviated magnetic field lines of the Earth. They are able to do this in the dark and by apparently seeking to maintain a specific angle with respect to the magnetic field vector. When the horizontal component of the magnetic vector was eliminated, animals became disoriented, and orientation became random. We infer that the animals observed had learned to prefer a particular magnetic direction following environmental/geographical cues. Alternatively, the magnetic directional alignments are innate as, e.g. in migrating birds, but these may be modified/altered according to season, age, hormonal status, and environmental factors such as “landmarks”, light-, sound-, or olfactory cues. Numerous observations of the aligning showed that the preference for a certain magnetic compass direction/axis was not only individual but also specific for the population-subgroups tested. Specimens roughly preferred magnetic directions close to east or west. However, the larvae were able to learn to align to obviously attractive hiding spots (tubes) that were provided in a direction that deviated with respect to the first magnetic preference. The new conditioned alignments were, again, referred to magnetically by the animals and remained stable, even if the hiding tubes were absent. Animals preferred that direction until, eventually, a new directional cue became attractive.