Migratory birds use head scans to detect the direction of the earth's magnetic field

Night-migratory songbirds are known to use a magnetic compass , but how do they detect the reference direction provided by the geomagnetic field, and where is the sensory organ located? The most prominent characteristic of geomagnetic sensory input, whether based on visual patterns or magnetite-mediated forces , is the predicted symmetry around the north-south or east-west magnetic axis. Here, we show that caged migratory garden warblers perform head-scanning behavior well suited to detect this magnetic symmetry plane. In the natural geomagnetic field, birds move toward their migratory direction after head scanning. In a zero-magnetic field , where no symmetry plane exists, the birds almost triple their head-scanning frequency, and the movement direction after a head scan becomes random. Thus, the magnetic sensory organ is located in the bird's head, and head scans are used to locate the reference direction provided by the geomagnetic field.     

Compass orientation and possible migration routes of passerine birds at high arctic latitudes

The use of celestial or geomagnetic orientation cues can lead migratory birds along different migration routes during the migratory journeys, e.g. great circle routes (approximate), geographic or magnetic loxodromes. Orientation cage experiments have indicated that migrating birds are capable of detecting magnetic compass information at high northern latitudes even at very steep angles of inclination. However, starting a migratory journey at high latitudes and following a constant magnetic course often leads towards the North Magnetic Pole, which means that the usefulness of magnetic compass orientation at high latitudes may be questioned. Here, we compare possible long‐distance migration routes of three species of passerine migrants breeding at high northern latitudes. The initial directions were based on orientation cage experiments performed under clear skies and simulated overcast and from release experiments under natural overcast skies. For each species we simulated possible migration routes (geographic loxodrome, magnetic loxodrome and sun compass route) by extrapolating from the initial directions and assessing a fixed orientation according to different compass mechanisms in order to investigate what orientation cues the birds most likely use when migrating southward in autumn. Our calculations show that none of the compass mechanisms (assuming fixed orientation) can explain the migration routes followed by night‐migrating birds from their high Nearctic breeding areas to the wintering sites further south. This demonstrates that orientation along the migratory routes of arctic birds (and possibly other birds as well) must be a complex process, involving different orientation mechanisms as well as changing compass courses. We propose that birds use a combination of several compass mechanisms during a migratory journey with each of them being of a greater or smaller importance in different parts of the journey, depending on environmental conditions. We discuss reasons why birds developed the capability to use magnetic compass information at high northern latitudes even though following these magnetic courses for any longer distance will lead them along totally wrong routes. Frequent changes and recalibrations of the magnetic compass direction during the migratory journey are suggested as a possible solution.     

Magnetic information calibrates celestial cues during migration

Migratory birds use celestial and geomagnetic directional information to orient on their way between breeding and wintering areas. Cue-conflict experiments involving these two orientation cue systems have shown that directional information can be transferred from one system to the other by calibration. We designed experiments with four species of North American songbirds to: (1) examine whether these species calibrate orientation information from one system to the other; and (2) determine whether there are species-specific differences in calibration. Migratory orientation was recorded with two different techniques, cage tests and free-flight release tests, during autumn migration. Cage tests at dusk in the local geomagnetic field revealed species-specific differences: red-eyed vireo, Vireo olivaceus, and northern waterthrush, Seiurus noveboracensis, selected seasonally appropriate southerly directions whereas indigo bunting, Passerina cyanea, and grey catbird, Dumetella carolinensis, oriented towards the sunset direction. When tested in deflected magnetic fields, vireos and waterthrushes responded by shifting their orientation according to the deflection of the magnetic field, but buntings and catbirds failed to show any response to the treatment. In release tests, all four species showed that they had recalibrated their star compass on the basis of the magnetic field they had just experienced in the cage tests. Since release tests were done in the local geomagnetic field it seems clear that once the migratory direction is determined, most likely during the twilight period, the birds use their recalibrated star compass for orientation at departure. Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

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 orientation: effects of cue-conflict experiments with young migratory songbirds in the high Arctic

The migratory orientation of juvenile white-crowned sparrows, Zonotrichia leucophrys gambelli, was investigated by orientation cage experiments in manipulated magnetic fields performed during the evening twilight period in northwestern Canada in autumn. We did the experiments under natural clear skies in three magnetic treatments: (1) in the local geomagnetic field; (2) in a deflected magnetic field (mN shifted −90°); and (3) after exposure to a deflected magnetic field (mN −90°) for 1 h before the cage experiment performed in the local geomagnetic field at dusk. Subjects showed a mean orientation towards geographical east in the local geomagnetic field, north of the expected migratory direction towards southeast. The sparrows responded consistently to the shifted magnetic field, demonstrating the use of a magnetic compass during their first autumn migration. Birds exposed to a cue conflict for 1 h on the same day before the experiment, and tested in the local geomagnetic field at sunset, showed the same northerly orientation as birds exposed to a shifted magnetic field during the experiment. This result indicates that information transfer occurred between magnetic and celestial cues. Thus, the birds' orientation shifted relative to available sunset and geomagnetic cues during the experimental hour. The mean orientation of birds exposed to deflected magnetic fields prior to and during testing was recorded up to two more times in the local geomagnetic field under natural clear and overcast skies before release, resulting in scattered mean orientations.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Magnetic Orientation in the Savannah Sparrow

Although magnetic compass orientation has been reported in a number of invertebrate and vertebrate taxa, including about a dozen migratory bird species, magnetic orientation capabilities in animals remain somewhat controversial. We have hand-raised a large number of Savannah sparrows (Passerculus sandwichensis) to study the ontogeny of orientation behavior. Young birds with a variety of early experience with visual and magnetic orientation cues have been tested for magnetic orientation during their first autumn migration. Here we present data from 80 hand-raised sparrows, each tested several times in both normal and shifted magnetic fields. Birds reared indoors with no experience with visual orientation cues showed axial north-south orientation that shifted by almost exactly the magnitude of 90° clockwise and counterclockwise shifts in the direction of magnetic north. Other groups of birds with varying early experience with visual orientation cues showed different preferred orientation directions, but all groups shifted orientation direction in response to shifts in the magnetic field. The data thus demonstrate a robust magnetic orientation ability in this species.     

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.     

Shifted magnetic fields lead to deflected and axial orientation of migrating robins,Erithacus rubecula,at sunset

The migratory orientation of the robin was tested in shifted magnetic fields during the twilight period after sunset, under clear skies and under simulated total overcast. The horizontal direction of the geomagnetic field was shifted 90° to the right or left in relation to the local magnetic field, without changing either the intensity of the field or its angle of inclination. Experiments were conducted during both spring and autumn, with robins captured as passage migrants at the Falsterbo and Ottenby bird observatories in southern Sweden as test subjects. Generally, the orientation of robins was affected by magnetic shifts compared to controls tested in the natural geomagnetic field. Autumn birds from the two capture sites differed in their responses, probably because of different migratory dispositions and body conditions. The robins most often changed their orientation to maintain their typical axis of migration relative to the shifted magnetic fields. However, preferred directions in relation to the shifted magnetic fields were frequently reverse from normal, or axial rather than unimodal. These results disagree with suggested mechanisms for orientation by visual sunset cues and with the proposed basis of magnetic orientation. They do, however, demonstrate that the geomagnetic field is involved in the sunset orientation of robins, probably in combination with additional visual or non-visual cues that contribute to establish magnetic polarity.     

Evidence for calibration of magnetic migratory orientation in Savannah sparrows reared in the field

The orientation system of migratory birds consists of a magnetic compass and compasses based upon celestial cues. In many places, magnetic compass directions and true or geographic compass directions differ (referred to as magnetic declination). It has been demonstrated experimentally in several species that the innate preferred direction of magnetic orientation can be calibrated by celestial rotation, an indicator of geographic directions. This calibration process brings the two types of compass into conformity and provides the birds with a mechanism that compensates for the spatial variation in magnetic declination. Calibration of magnetic orientation has heretofore been demonstrated only with hand-raised birds exposed to very large declination (90° or more). Here we show that the magnetic orientation of wild birds from near Albany, New York, USA (declination = 14° W) was N–S, a clockwise shift of 26° from the NNW–SSE direction of birds raised entirely indoors. Hand-raised birds having visual experience with either the daytime sky or both day and night sky orientated N–S, similar to wild-caught birds. These data provide the first confirmation that calibration of magnetic orientation occurs under natural conditions and in response to modest declination values.     

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.     

The osmotic magnetometer: a new model for magnetite-based magnetoreceptors in animals

Homing pigeons and migratory birds are well known examples for animals that use the geomagnetic field for their orientation. Yet, neither the underlying receptor mechanism nor the magnetoreceptor itself is known. Recently, an innervated structure containing clusters of magnetite nanocrystals was identified in the upper beak skin of the homing pigeon. Here we show theoretically that such a cluster has a magnetic-field-dependent shape, even in fields as weak as the Earth's magnetic field; by converting magnetic stimuli into mechanical strain, the clusters can be assumed as primary units of magnetoperception in homing pigeons. Since the orientation of the strain ellipsoid indicates the direction of the external magnetic field, a cluster of magnetite nanocrystals also has the potential to serve as the basis of the so-called inclination compass of migratory birds. It is quantitatively demonstrated that the magnetic-field-induced shape change of a cluster can be amplified as well as counterbalanced by means of osmotic pressure regulation, which offers an elegant possibility to determine the magnetic field strength just by measuring changes in concentration. Received: 18 May 1998 / Revised version: 11 February 1999 / Accepted: 11 February 1999     

Magnetic compass orientation research with migratory songbirds at Stensoffa Ecological Field Station in southern Sweden: why is it so difficult to obtain seasonally appropriate orientation?

More than three decades ago, Thomas Alerstam initiated the study of orientation and navigation of migratory songbirds in southern Sweden. Stensoffa Ecological Field Station, located approx. 20 km east of Lund, has since been a primary location for orientation experiments. However, it has often been difficult to record well‐oriented behaviour in the seasonal appropriate migratory directions, in particular in magnetic orientation experiments under simulated overcast or indoors. Here, we summarise all available experiments testing magnetic compass orientation in migratory songbirds in southern Sweden, and review possible explanations for the poor magnetic compass orientation found in many studies. Most of the factors proposed can be essentially excluded, such as difficulties to extract magnetic compass information at high latitudes, methodological or experimenter biases, holding duration and repeated testing of individual birds, effects of magnetic anomalies and temporal variations of the ambient magnetic field, as well as anthropogenic electromagnetic disturbances. Possibly, the geographic location of southern Sweden where many birds captured and/or tested at coastal sites are confronted with the sea, might explain some of the variation that we see in the orientation behaviour of birds. Still, further investigations are needed to conclusively identify the factors responsible for why birds are not better oriented in the seasonal appropriate migratory direction at Stensoffa.     

Orientation of Dunnocks (Prunella modularis) at Sunset

To find out the relative importance of the geomagnetic and solar cues for the orientation at the time of sunset, dunnocks were tested outdoors during the spring migration periods of 1982 and 1983. Experimental magnetic fields were produced by Helmholtz coils. In the various magnetic conditions, the following results were obtained:

• 1 In the local geomagnetic field, the dunnocks oriented in a seasonally appropriate northerly direction.
• 2 In a magnetic field the north of which was shifted 120° clock-wise to ESE, the birds showed a corresponding shift in their orientation.
• 3 In a vertical magnetic field without meaningful directional information, birds previously tested in either the local geomagnetic field or the shifted magnetic field now displayed axially bimodal orientation, with the axes of the two groups differing.

These findings indicate that for migratory dunnocks, the magnetic field plays a dominant role in determining their orientation at the time of sunset, and that magnetic information may affect the dunnocks' response to other directional, presumably solar cues as well.     

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.     

The ontogeny of orientation in young pigeons

When young pigeons begin to fly, their only means of orientation appears to be a magnetic compass provided by their innate ability to perceive the geomagnetic field. This magnetic compass enables the birds to calibrate other potential orientation stimuli found in their environment thus establishing complex learned mechanisms of orientation preferentially used by experienced birds, like the sun compass and the navigational “map”. The learning processes are described and discussed.     

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.     

Interaction of magnetite-based receptors in the beak with the visual system underlying 'fixed direction' responses in birds

Background

European robins, Erithacus rubecula, show two types of directional responses to the magnetic field: (1) compass orientation that is based on radical pair processes and lateralized in favor of the right eye and (2) so-called 'fixed direction' responses that originate in the magnetite-based receptors in the upper beak. Both responses are light-dependent. Lateralization of the 'fixed direction' responses would suggest an interaction between the two magnetoreception systems.

Results

Robins were tested with either the right or the left eye covered or with both eyes uncovered for their orientation under different light conditions. With 502 nm turquoise light, the birds showed normal compass orientation, whereas they displayed an easterly 'fixed direction' response under a combination of 502 nm turquoise with 590 nm yellow light. Monocularly right-eyed birds with their left eye covered were oriented just as they were binocularly as controls: under turquoise in their northerly migratory direction, under turquoise-and-yellow towards east. The response of monocularly left-eyed birds differed: under turquoise light, they were disoriented, reflecting a lateralization of the magnetic compass system in favor of the right eye, whereas they continued to head eastward under turquoise-and-yellow light.

Conclusion

'Fixed direction' responses are not lateralized. Hence the interactions between the magnetite-receptors in the beak and the visual system do not seem to involve the magnetoreception system based on radical pair processes, but rather other, non-lateralized components of the visual system.     

The Direction of Celestial Rotation Affects the Development of Migratory Orientation in Pied Flycatchers,Ficedula hypoleuca

The migratory direction in young passerine migrants is based on innate information, with the geomagnetic field and celestial rotation as references. To test whether the direction of celestial rotation is of importance, hand-raised pied flycatchers in Latvia were exposed during the premigratory period to a planetarium rotating in different directions. During autumn migration, when their orientation behavior was recorded in the local geomagnetic field in the absence of celestial cues, birds that had been exposed to a sky rotating in the natural direction showed a unimodal preference of their south-westerly migratory direction. Birds that had been exposed to a sky rotating in the reversed direction, in contrast, showed a bimodal preference of an axis south-west-north-east. Their behavior was similar to that of pied flycatchers that had been raised without access to celestial cues. In Latvia, the magnetic field alone allows only orientation along the migratory axis, and celestial rotation enables birds to select the correct end of this axis. Our findings show that the direction of rotation is of crucial importance: celestial rotation is effective only if the stars move in the natural direction.     

Orientation by magnetic field in leaf-cutter ants, Atta colombica (Hymenoptera: Formicidae)

Leaf‐cutter ants (Atta colombica) use trail following to travel between foraging sites and the home nest. However, this combination of pheromone and visual cues is likely to be complemented by a directional reference system such as a compass, used not only when foraging but also during colony formation, where foraging trails degrade or where ants become displaced. One candidate system is the magnetic polarity compass. We tested the orientation of leaf‐cutter ants under a magnetic field of reversed‐polarity, with the prediction that the ants would show 180° deflection compared with control ants in an unchanged geomagnetic field. When the sun's disc was unobstructed by clouds, orientation was the same as that of control ants, implying that magnetic cues were not used to orient. However, when the sky was overcast, ants in the experimental treatment significantly shifted their mean orientation both in comparison with controls and reversed‐polarity ants under the sun. Although a total reversal in orientation was not induced, the results demonstrate that Atta respond to magnetic reversal in the absence of sunlight cues, and suggest a role for magnetic cues in determining direction during orientation.