鸟类磁感受的生物物理机制研究进展

行为学实验表明,许多鸟类能够感受到地磁信息,并利用地磁信息完成迁徙或归巢。地磁场信息能提供可靠导航信息,磁力线可提供罗盘信息,而磁场强度和倾角可提供位置信息。文章介绍了鸟类磁感受机制的两种重要假说——基于磁铁矿的磁感受假说和化学磁感受假说,阐明了两种假说的理论原理及实验证据,对地磁信息传导神经通路与处理脑区做了评述,并展望了其发展方向。     

Electroretinographic study of the magnetic compass in European robins

Migratory birds are known to be sensitive to external magnetic field (MF). Much indirect evidence suggests that the avian magnetic compass is localized in the retina. Previously, we showed that changes in the MF direction could modulate retinal responses in pigeons. In the present study, we performed similar experiments using the traditional model animal to study the magnetic compass, European robins. The photoresponses of isolated retina were recorded using ex vivo electroretinography (ERG). Blue- and red-light stimuli were applied under an MF with the natural intensity and two MF directions, when the angle between the plane of the retina and the field lines was 0° and 90°, respectively. The results were separately analysed for four quadrants of the retina. A comparison of the amplitudes of the a- and b-waves of the ERG responses to blue stimuli under the two MF directions revealed a small but significant difference in a- but not b-waves, and in only one (nasal) quadrant of the retina. The amplitudes of both the a- and b-waves of the ERG responses to red stimuli did not show significant effects of the MF direction. Thus, changes in the external MF modulate the European robin retinal responses to blue flashes, but not to red flashes. This result is in a good agreement with behavioural data showing the successful orientation of birds in an MF under blue, but not under red illumination.     

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.     

Das Orientierungssystem der V?gel I. Kompa?mechanismen

Zusammenfassung V?gel stellen den Bezug zum Ziel indirekt über ein externes Referenzsystem her. Der Navigationsproze? besteht deshalb aus zwei Schritten: zun?chst wird die Richtung zum Ziel als Kompa?kurs festgelegt, dann wird dieser Kurs mit Hilfe eines Kompa?mechanismus aufgesucht. Das Magnetfeld der Erde und Himmelsfaktoren werden von den V?gel als Kompa? benutzt. In der vorliegenden Arbeit werden der Magnetkompa?, der Sonnenkompa? und der Sternkompa? der V?gel in ihrer Funktionsweise, ihrer Entstehung und ihrer biologischen Bedeutung vorgestellt. Der Magnetkompa? erwies sich als Inklinationskompa?, der nicht auf der Polarit?t, sondern auf der Neigung der Feldlinien im Raum beruht; er unterscheidet „polw?rts“ und „?quatorw?rts“ statt Nord und Süd. Er ist ein angeborener Mechanismus und wird beim Vogelzug und beim Heimfinden benutzt. Seine eigentliche Bedeutung liegt jedoch darin, da? er ein Referenzsystem bereitstellt, mit dessen Hilfe andere Orientierungsfaktoren zueinander in Beziehung gesetzt werden k?nnen. Der Sonnenkompa? beruht auf Erfahrung; Sonnenazimut, Tageszeit und Richtung werden durch Lernprozesse miteinander verknüpft, wobei der Magnetkompa? als Richtungsreferenzsystem dient. Sobald er verfügbar ist, wird der Sonnenkompa? bei der Orientierung im Heimbereich und beim Heimfinden bevorzugt benutzt; beim Vogelzug spielt er, wahrscheinlich wegen seiner Abh?ngigkeit von der geographischen Breite, kaum eine Rolle. Der Sternkompa? arbeitet ohne Beteiligung der Inneren Uhr; die V?gel leiten Richtungen aus den Konfigurationen der Sterne zueinander ab. Lernprozesse erstellen den Sternkompa? in der Phase vor dem ersten Zug; dabei fungiert die Himmelsrotation als Referenzsystem. Sp?ter, w?hrend des Zuges, übernimmt der Magnetkompa? diese Rolle. Die relative Bedeutung der verschiedenen Kompa?systeme wurde in Versuchen untersucht, bei denen Magnetfeld und Himmelsfaktoren einander widersprechende Richtungs-information gaben. Die erste Reaktion der V?gel war von Art zu Art verschieden; langfristig scheinen sich die V?gel jedoch nach dem Magnetkompa? zu richten. Dabei werden die Himmelsfaktoren umgeeicht, so da? magnetische Information und Himmelsinformation wieder im Einklang stehen. Der Magnetkompa? und die Himmelsfaktoren erg?nzen einander: der Magnetkompa? ersetzt Sonnen- und Sternkompa? bei bedecktem Himmel; die Himmelsfaktoren erleichtern den V?geln das Richtungseinhalten, zu dem der Magnetkompa? offenbar wenig geeignet ist. Magnetfeld und Himmelsfaktoren sollten deshalb als integrierte Komponenten eines multifaktoriellen Systems zur Richtungsorientierung betrachtet werden.

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The orientation system of birds — I. Compass mechanisms

Summary Because of the large distances involved, birds establish contact with their goal indirectly via an external reference. Hence any navigation is a two-step process: in the first step, the direction to the goal is determined as a compass course; in the second step, this course is located with a compass. The geomagnetic field and celestial cues provide birds with compass information. The magnetic compass of birds, the sun compass the star compass and the interactions between the compass mechanisms are described in the present paper. Magnetic compass orientation was first demonstrated by testing night-migrating birds in experimentally altered magnetic fields: the birds changed their directional tendencies according to the deflected North direction. The avian magnetic compass proved to be an inclination compass: it does not use polarity; instead it is based on the axial course of the field lines and their inclination in space, distinguishing “poleward” and “equatorward” rather than North and South. Its functional range is limited to intensities around the local field strength, but this biological window is flexible and can be adjusted to other intensities. The magnetic compass is an innate mechanism that is widely used in bird migration and in homing. Its most important role, however, is that of a basic reference system for calibrating other kinds of orientation cues. Sun compass orientation is demonstrated by clock-shift experiments: Shifting the birds' internal clock causes them to misjudge the position of the sun, thus leading to typical deflections which indicate sun compass use. The analysis of the avian sun compass revealed that it is based only on sun azimuth and the internal clock; the sun's altitude is not involved. The role of the pattern of polarized light associated with the sun is unclear; only at sunset has it been shown to be an important cue for nocturnal migrants, being part of the sun compass. The sun compass is based on experience; sun azimuth, time of day and direction are combined by learning processes during a sensitive period, with the magnetic compass serving as directional reference. When established, the sun compass becomes the preferred compass mechanism for orientation tasks within the home region and homing: in migration, however, its role is minimal, probably because of the changes of the sun's arc with geographic latitude. The star compass was demonstrated in night-migrating birds by projecting the northern stars in different directions in a planetarium. The analysis of the mechanism revealed that the internal clock is not involved; birds derive directions from the spatial relationship of the star configurations. The star compass is also established by experience; the directional reference is first provided by celestial rotation, later, during migration, by the magnetic compass. The relative importance of the various compass mechanisms has been tested in experiments in which celestial and magnetic cues gave conflicting information. The first response of birds to conflicting cues differs considerably between species; after repeated exposures, however, the birds oriented according to magnetic North, indicating a long-term dominance of the magnetic compass. Later tests in the absence of magnetic information showed that celestial cues were not simply ignored, but recalibrated so that they were again in agreement with magnetic cues. The magnetic compass and celestial cues complement each other: the magnetic field ensures orientation under overcast sky; celestial cues facilitate maintaining directions, for which the magnetic compass appears to be ill suited. In view of this, the magnetic field and celestial cues should be regarded as integrated components of a multifactorial system for directional orientation.

     

Migratory Orientation: Magnetic Compass Orientation of Garden Warblers (Sylvia borin) after a Simulated Crossing of the Magnetic Equator

Since the birds' magnetic compass works as an inclination compass using the axial course of the magnetic field lines and their inclination, transequatorial migrants have to reverse their reaction with respect to the magnetic field after crossing the magnetic equator. Garden Warblers, long distance migrants breeding in Europe and wintering in tropical and southern Africa, were tested during autumn in the local geomagnetic field on the northern hemisphere. The experimental group was exposed to a field with horizontal field lines, simulating equator crossing, at the beginning of October; afterwards the birds were tested in the local geomagnetic field again. While the controls showed southerly tendencies during the entire season, the experimentals reversed their directional tendencies after staying in the horizontal field and now preferred northerly directions. In a field of the southern hemisphere, this preference corresponds to a southern course which would have meant the continuation of their migration flight.     

Do release-site biases reflect response to the Earth's magnetic field during position determination by homing pigeons?

How homing pigeons (Columba livia) return to their loft from distant, unfamiliar sites has long been a mystery. At many release sites, untreated birds consistently vanish from view in a direction different from the home direction, a phenomenon called the release-site bias. These deviations in flight direction have been implicated in the position determination (or map) step of navigation because they may reflect local distortions in information about location that the birds obtain from the geophysical environment at the release site. Here, we performed a post hoc analysis of the relationship between vanishing bearings and local variations in magnetic intensity using previously published datasets for pigeons homing to lofts in Germany. Vanishing bearings of both experienced and naïve birds were strongly associated with magnetic intensity variations at release sites, with 90 per cent of bearings lying within ±29° of the magnetic intensity slope or contour direction. Our results (i) demonstrate that pigeons respond in an orderly manner to the local structure of the magnetic field at release sites, (ii) provide a mechanism for the occurrence of release-site biases and (iii) suggest that pigeons may derive spatial information from the magnetic field at the release site that could be used to estimate their current position relative to their loft.     

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.     

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.     

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.     

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.     

A visual pathway links brain structures active during magnetic compass orientation in migratory birds

The magnetic compass of migratory birds has been suggested to be light-dependent. Retinal cryptochrome-expressing neurons and a forebrain region, "Cluster N", show high neuronal activity when night-migratory songbirds perform magnetic compass orientation. By combining neuronal tracing with behavioral experiments leading to sensory-driven gene expression of the neuronal activity marker ZENK during magnetic compass orientation, we demonstrate a functional neuronal connection between the retinal neurons and Cluster N via the visual thalamus. Thus, the two areas of the central nervous system being most active during magnetic compass orientation are part of an ascending visual processing stream, the thalamofugal pathway. Furthermore, Cluster N seems to be a specialized part of the visual wulst. These findings strongly support the hypothesis that migratory birds use their visual system to perceive the reference compass direction of the geomagnetic field and that migratory birds "see" the reference compass direction provided by the geomagnetic field.     

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.     

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.     

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.     

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.     

Wintergoldh?hnchen (Regulus regulus) besitzen einen Inklinationskompa?

During autumn migration, orientation tests were performed with Goldcrests in the morning immediately after the birds had been caught. In the local geomagnetic field (vertical component pointing downward), they showed a significant tendency towards 144° SE; in a magnetic field with the vertical component pointing upward, their mean was at 321° NW. This response to an inversion of the vertical component reveals that the Goldcrests used the magnetic field for orientation and that their magnetic compass is an inclination compass as it has been described for several other species of migrants.     

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.     

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 .     

Bats Respond to Very Weak Magnetic Fields

How animals, including mammals, can respond to and utilize the direction and intensity of the Earth’s magnetic field for orientation and navigation is contentious. In this study, we experimentally tested whether the Chinese Noctule, Nyctalus plancyi (Vespertilionidae) can sense magnetic field strengths that were even lower than those of the present-day geomagnetic field. Such field strengths occurred during geomagnetic excursions or polarity reversals and thus may have played an important role in the evolution of a magnetic sense. We found that in a present-day local geomagnetic field, the bats showed a clear preference for positioning themselves at the magnetic north. As the field intensity decreased to only 1/5^th of the natural intensity (i.e., 10 μT; the lowest field strength tested here), the bats still responded by positioning themselves at the magnetic north. When the field polarity was artificially reversed, the bats still preferred the new magnetic north, even at the lowest field strength tested (10 μT), despite the fact that the artificial field orientation was opposite to the natural geomagnetic field (P<0.05). Hence, N. plancyi is able to detect the direction of a magnetic field even at 1/5th of the present-day field strength. This high sensitivity to magnetic fields may explain how magnetic orientation could have evolved in bats even as the Earth’s magnetic field strength varied and the polarity reversed tens of times over the past fifty million years.     

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.