The role of the sun in the celestial compass of dung beetles

Recent research has focused on the different types of compass cues available to ball-rolling beetles for orientation, but little is known about the relative precision of each of these cues and how they interact. In this study, we find that the absolute orientation error of the celestial compass of the day-active dung beetle Scarabaeus lamarcki doubles from 16° at solar elevations below 60° to an error of 29° at solar elevations above 75°. As ball-rolling dung beetles rely solely on celestial compass cues for their orientation, these insects experience a large decrease in orientation precision towards the middle of the day. We also find that in the compass system of dung beetles, the solar cues and the skylight cues are used together and share the control of orientation behaviour. Finally, we demonstrate that the relative influence of the azimuthal position of the sun for straight-line orientation decreases as the sun draws closer to the horizon. In conclusion, ball-rolling dung beetles possess a dynamic celestial compass system in which the orientation precision and the relative influence of the solar compass cues change over the course of the day.     

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.

     

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 Compass Orientation in the European Eel

European eel migrate from freshwater or coastal habitats throughout Europe to their spawning grounds in the Sargasso Sea. However, their route (∼ 6000 km) and orientation mechanisms are unknown. Several attempts have been made to prove the existence of magnetoreception in Anguilla sp., but none of these studies have demonstrated magnetic compass orientation in earth-strength magnetic field intensities. We tested eels in four altered magnetic field conditions where magnetic North was set at geographic North, South, East, or West. Eels oriented in a manner that was related to the tank in which they were housed before the test. At lower temperature (under 12°C), their orientation relative to magnetic North corresponded to the direction of their displacement from the holding tank. At higher temperatures (12–17°C), eels showed bimodal orientation along an axis perpendicular to the axis of their displacement. These temperature-related shifts in orientation may be linked to the changes in behavior that occur between the warm season (during which eels are foraging) and the colder fall and winter (during which eels undertake their migrations). These observations support the conclusion that 1. eels have a magnetic compass, and 2. they use this sense to orient in a direction that they have registered moments before they are displaced. The adaptive advantage of having a magnetic compass and learning the direction in which they have been displaced becomes clear when set in the context of the eel’s seaward migration. For example, if their migration is halted or blocked, as it is the case when environmental conditions become unfavorable or when they encounter a barrier, eels would be able to resume their movements along their old bearing when conditions become favorable again or when they pass by the barrier.     

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.     

Spectral information as an orientation cue in dung beetles

During the day, a non-uniform distribution of long and short wavelength light generates a colour gradient across the sky. This gradient could be used as a compass cue, particularly by animals such as dung beetles that rely primarily on celestial cues for orientation. Here, we tested if dung beetles can use spectral cues for orientation by presenting them with monochromatic (green and UV) light spots in an indoor arena. Beetles kept their original bearing when presented with a single light cue, green or UV, or when presented with both light cues set 180° apart. When either the UV or the green light was turned off after the beetles had set their bearing in the presence of both cues, they were still able to maintain their original bearing to the remaining light. However, if the beetles were presented with two identical green light spots set 180° apart, their ability to maintain their original bearing was impaired. In summary, our data show that ball-rolling beetles could potentially use the celestial chromatic gradient as a reference for orientation.     

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.     

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.     

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.     

Learned orientation in landward swimming in the cricket Pteronemobius Lineolatus

Pteronemobius lineolatus swims landward visually guided by terrestrial and, at times, associated celestial cues.Crickets irrespective of their previous visual experience swim towards artificial black horizontal landmarks. Non shore-dwelling crickets select random directions when released, under blue sky, for the first time on water surface in the absence of landmarks. If old enough to swim larvae and adult crickets learn a compass direction, during their first swim and each new directional landward swimming, if there are conspicuous terrestrial landmarks.There is forgetting and relearning of celestial compass orientation.     

Orientation in a desert lizard (Uma notata): time-compensated compass movement and polarotaxis

Summary The diurnal escape response of fringetoed lizards (Uma notata) startled by predators demonstrates clear directional orientation not likely to depend on local landmarks in the shifting sands of their desert environment. Evidence that celestial orientation is involved in this behavior has been sought in the present experiments by testing the effects of (1) phase shifting the animal's internal clock by 6 h and (2) by training the lizards to seek shelter while exposed to natural polarization patterns. In the first case, 90° shifts in escape direction were demonstrated in outdoor tests, as expected if a time-compensated sun or sky polarized light compass is involved. In the second instance, significant bimodale-vector dependent orientation was found under an overhead polarizing light filter but this was only evident when the response data were transposed to match the zenithe-vector rotation dependent on the sun's apparent movement through the sky. This extends to reptiles the capacity to utilize overheade-vector directions as a time-compensated sky compass. The sensory site of this discrimination and the relative roles of sun and sky polarization in nature remain to be discovered.     

Das Orientierungssystem der V?gel III. Zugorientierung

Zusammenfassung Viele Zugvögel sind ortstreu; sie brüten und überwintern wiederholt am gleichen Ort. Die Zugwege sind an die Bedingungen zwischen Brutgebiet und Winter angepaßt, was oft zu nicht-gradlinigen Routen führt. Junge Zugvögel auf dem ersten Zug erreichen das ihnen noch unbekannte Winterquartier aufgrund angeborener Information über Richtung und Entfernung, wobei die Entfernung durch ein endogenes Zeitprogramm gesteuert wird, das Menge und Verlauf der Zugaktivität vorgibt.Die Vögel bedienen sich zweier Referenzsysteme, um die genetisch kodierte Richtungsinformation in eine aktuelle Flugrichtung umzusetzen: der Himmelsrotation und des Erdmagnetfelds. Die von ersterer bereitgestellte Referenzrichtung liegt gegenüber dem Rotationszentrum, entspricht geographisch Süd und wird durch Beobachtung des Tag- und Nachthimmels ermittelt. Mit ihrer Hilfe wird ein Sternkompaß aufgebaut. Vögel, die normalerweise nach Südwesten ziehen, bevorzugten, wenn ihnen nur Himmelsmarken zur Verfügung standen, rein südliche Richtungen. Sie waren jedoch in ihrer populationsspezifischen Zugrichtung orientiert, wenn ihnen nur magnetische Information zur Verfügung stand. Ausnahmen wurden in Gebieten mit steiler Inklination beobachtet, wo das Magnetfeld allein nur eine Achse vorgibt und die Vögel zur eindeutigen Orientierung zusätzlich Information von der Himmelsrotation benötigen. Da der Magnetkompaß als Inklinationskompaß arbeitet, können die Zugvögel der Nord- und der Südhalbkugel das gleiche Zugprogramm benutzen: im Herbst fliegen sie äquatorwärts.Zwischen den beiden Referenzsystemen treten Wechselwirkungen auf. Wenn das Rotationszentrum des Himmels und magnetisch Nord divergieren, dominiert während der prämigratorischen Phase die Himmelsrotation, und der magnetische Kurs wird umgestellt. Dabei gibt die Himmelsrotation nur eine Referenzrichtung vor; die populationsspezifische Abweichung von dieser Richtung ist nur in bezug auf das Magnetfeld kodiert und wird dann hinzugefügt. Der Grund, hier zwei Referenzsysteme zu benutzen, liegt wahrscheinlich darin, daß das Magnetfeld in höheren Breiten stark von der Säkularvariation beeinflußt wird, gleichzeitig aber, da es direkt wahrgenommen werden kann, vielleicht besser zur Kodierung von Richtungsabweichungen geeignet ist.Während des eigentlichen Zuges ist dagegen das Magnetfeld dominant. Im Konfliktfall werden Sterne und Sonnenuntergangsfaktoren entsprechend der magnetischen Nordrichtung umgeeicht. Bei Vögeln, die auf dem Zug Richtungswechsel durchführen, ist der zweite Kurs in bezug auf das Magnetfeld kodiert und wird offenbar erst während des Zuges festgelegt. Bei Gartengrasmücken und Gelbgesichtshonigfressern scheint das endogene Zugprogramm allein den Kurswechsel einleiten zu können; Trauerschnäpper sind dagegen zusätzlich auf bestimmte magnetische Bedingungen angewiesen. Für Transäquatorialzieher bewirkt der horizontale Feldlinienverlauf am magnetischen Äquator eine Richtungsumkehr von äquatorwärts nach polwärts.Das angeborene Zugprogramm führt junge Zugvögel in ihr Überwinterungsgebiet; es wird gegen Ende flexibel und erlaubt ihnen, sich einen geeigneten Ort als ihr Winterquartier zu suchen. Für den Zug zurück ins Brutgebiet und alle späteren Zugbewegungen können Vögel zusätzlich auf unterwegs gewonnene Erfahrungen zurückgreifen. Die vom angeborenen Zugprogramm weiterhin zur Verfügung gestellte Richtungsinformation wird durch auf Ortsinformation beruhende Navigationsvorgänge ergänzt und ersetzt. Dies erlaubt erfahrenen Zugvögeln z. B., günstige Rastgebiete gezielt wieder aufzusuchen, und macht sie weniger anfällig gegen Winddrift. Die Zugorientierung zeigt hier eine Parallele zum Heimfinden: sobald erfahrungsabhängige Mechanismen zur Verfügung stehen, werden diese gegenüber den angeborenen Mechanismen bevorzugt.

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The orientation system of birds — III. Migratory orientation

Summary Many migratory birds show philopatry, i.e. they regularly breed and winter at the same sites. The routes taken by migrants are adjusted to the geographical and ecological conditions between breeding and wintering areas, often resulting in indirect paths. Young birds on their first migration face the task of reaching the as yet unknown population-specific winter quarters with the help of innate information. Large-scale displacement experiments with migrants and cage experiments with hand-raised birds revealed that this innate information is given as direction and distance, with the distance controlled by an endogenous time program that determines amount and temporal distribution of migratory activity. Both, migratory activity and direction — or, in the case of indirect routes, a sequence of directions — are genetically transmitted from one generation to the next.Birds use two reference systems to convert innate directional information into an actual flying course: celestial rotation and the geomagnetic field. Celestial rotation produces a reference direction opposite from its center, which is obtained by observing the diurnal and/or the nocturnal sky. This reference can be used to establish a star compass, not only utilizing the natural, but also artificial stars, provided the birds can observe these stars rotating. However, with only stars available, migrants that normally prefer southwesterly courses show southerly tendencies, apparently unable to convert the population-specific components of their migratory direction. Birds raised with only magnetic cues available, in contrast, are well oriented in their population-specific migratory direction, except in areas with steep inclination; here, the magnetic field provides only an axis, and birds also need celestial rotation for unimodal orientation. As the birds' magnetic compass is an inclination compass, migrants of the northern and southern hemisphere may use the same migratory program, starting out equatorwards in autumn.During the premigratory period, both reference systems interact to determine the migratory course. If North indicated by celestial rotation and magnetic North diverge, celestial rotation proves dominant, resulting in a changed magnetic compass course. However, celestial rotation does not simply override the magnetic course. In the natural situation, celestial rotation provides only the reference direction opposite from the center of rotation, corresponding to geographic South, which can be substituted by magnetic South if birds have no access to celestial cues. Population-specific deviations from South seem to be coded only with respect to the magnetic field and are then added to the reference direction, resulting in the population-specific migratory course. These processes are interrupted if the sky is made to rotate in the reverse direction. The reasons for using two reference systems may lie in the fact that at higher latitudes, the magnetic field is strongly affected by secular variations, while celestial rotation reliably provides geographic South. At the same time, the magnetic field, being directly perceivable, may be better suited for indicating angular deviations.During migration itself, the relationship between the two reference systems changes, with the magnetic field becoming dominant. In case of conflict, celestial cues are recalibrated according to magnetic North. The reasons for this shift in dominance may lie in celestial rotation ceasing to play a role. The sky changes its appearance as the birds progress, and the new stars are calibrated with the help of the geomagnetic field which becomes a reliable source of directional information at temperate and lower latitudes.Many birds change direction during migration. Their second compass course is coded with respect to the magnetic field. The conversion of the respective innate information appears to take place en route; a possible role of celestial rotation has not yet been analysed. In Garden Warblers and Yellow-faced Honeyeaters, the shift in direction can take place under the control of the endogenous time program alone; Pied Flycatchers, in contrast, require magnetic conditions of the region where the shift normally takes place. At the magnetic equator, birds must reverse their course with respect to their magnetic compass from equatorwards to polewards in order to continue southwards. Here, the field of the equator with its horizontal field lines serves as trigger. At the equator itself, where the magnetic compass becomes bimodal, birds may rely on celestial cues.The innate migratory program enables young birds to reach their general wintering area. The program becomes flexible at the end and allows them to look around for a suitable site to spend the winter. This becomes their winter home to which they return upon displacement. For the return migration to the breeding area and any later migrations, migratory birds can make use of experience obtained during earlier travels. The migratory program still provides them with directional information; however, navigational processes based on site-specific information dominate over the innate mechanisms. Many young birds undertake extended exploratory flights before they leave for migration, thus establishing a map of their future breeding area. As a consequence, they return to the normal breeding area after displacement. Adult birds must be expected to choose their migration route by mechanisms of true navigation, thus avoiding unfavorable areas and revisiting good refueling sites, at the same time becoming less vulnerable to wind drift and similar phenomena. Details of these navigation processes are not known, as they have escaped experimental analysis so far.The dominant role of true navigation, which replaces the innate program, represents a parallel to homing, where birds also rely on mechanisms of true navigation as soon as these become available.

     

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.     

Manipulations of polarized skylight calibrate magnetic orientation in a migratory bird

1. Young migratory birds enter the world with two representations of the migratory direction, one coded with respect to the magnetic field, the other with respect to celestial rotation. The preferred magnetic direction of migratory orientation is malleable early in life: it may be calibrated by celestial rotation, observed either in daytime or at night.
2. Previous experiments showed that early experience with skylight polarization was necessary for calilbration to occur in daytime. In this study, we performed a direct manipulation of patterns of polarized skylight at dawn and dusk.
3. Hand-raised Savannah sparrows (Passerculus sandwichensis) were allowed to observe the clear sky for 1 h prior to local sunrise and for one h following local sunset. They never saw the Sun nor stars. The birds observed the sky through bands of polarizing material (HNP'B) aligned with the e-vector axis in one of three orientations with respect of the azimuth of sunrise and sunset: group 1) 90°; group 2) 45° CW; group 3) 45° CCW.
4. Tested indoors in covered cages in both shifted and unshifted magnetic fields, the autumn migratory orientation of the three groups differed significantly. Group 1 oriented magnetic N-S, group 2 oriented magnetic NW-SE, and group 3 oriented magnetic NNE-SSW. These observed orientation directions are very close to those predicted by the manipulations of polarized skylight.
5. These results indicated that a fairly simplified, static polarized light pattern viewed a limited number of times only in dawn and dusk snapshots is sufficient to produce calibration of the preferred magnetic migratory orientation direction.

     

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.     

Magnetic versus celestial cues: cue-conflict experiments with migrating silvereyes at dusk

To assess the relative importance of celestial and magnetic cues for orientation at dusk, Australian silvereyes, Zosterops l. lateralis, were subjected to artificial magnetic fields under the natural evening sky, beginning 30 min before sunset. Control birds tested in the local geomagnetic field preferred their normal south-southwesterly migratory direction. Birds tested in a magnetic field with north deflected counterclockwise to 240°WSW showed northeasterly tendencies from the first test onward. Birds subjected to a corresponding clockwise deflection to 120°ESE, in contrast, first showed southerly directions, but from the 7th test onward shifted towards the northwest. Hence, both experimental groups followed the shift in magnetic north, one immediately, the other after a delay. When the birds were later tested in a vertical magnetic field without directional information, the two experimental groups continued in the direction they had preferred in the artificial magnetic fields, presumably by celestial cues alone. This indicates that they had not simply ignored celestial cues, but had recalibrated them according to the altered magnetic fields. The reasons for the initial difference between the two experimental groups remain unclear. Delayed responses to deflections of magnetic north have also been observed in previous studies. They appear to be the main reason why studies that expose birds only once to a cue-conflict situation often seem to indicate a dominance of celestial cues, whereas studies exposing the birds repeatedly usually indicate a dominance of magnetic cues. Accepted: 17 September 1997     

Orientation Cage and Release Experiments with Migratory Wheatears (Oenanthe oenanthe) in Scandinavia and Greenland: The Importance of Visual Cues

Migratory orientation of Scandinavian and Greenland wheatears was recorded during the autumn migration periods of 1988 and 1989. Orientation cage tests were conducted under clear sunset skies, to investigate the importance of different visible sky sections on orientation performance. In addition, wheatears were released under clear starry skies and under total overcast to examine the orientation of free-flying birds. The following results were obtained:

• 1 Wheatears tested with a restricted visible sky section (90° centered around zenith) in orientation cages, showed a mean orientation towards geographic W/geomagnetic NW (Greenland) and towards geographic and magnetic WNW-NW (Sweden). These mean directions are clearly inconsistent with the expected autumn migration directions, SW-SSW in Scandinavia and SE in Greenland, as revealed by ringing recoveries for the two populations.
• 2 When the birds were allowed a much more extensive view of the sky, almost down to the horizon (above 10° elevation), Scandinavian wheatears chose headings in agreement with ringing data. Greenland birds were not significantly oriented.
• 3 Release experiments under clear starry skies resulted in mean vanishing directions in good agreement with ringing data from both sites. Greenland wheatears released under total overcast showed a similar orientation as under clear skies, indicating that a view of the stars may not be of crucial importance for selecting a seasonally accurate migratory direction.

The results suggest that an unobstructed view of the sky, including visual cues low over the horizon, is important, possibly in combination with geomagnetic cues, for the orientation of migratory naive wheatears. Furthermore, the birds showed remarkably similar orientation responses in Greenland and Scandinavia, respectively, indicating that they use basically the same orientation system, despite considerable differences in visual and geomagnetic orientation premises at the two different geographic and magnetic latitudes.     

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.     

Dramatic orientation shift of white-crowned sparrows displaced across longitudes in the high Arctic

Advanced spatial-learning adaptations have been shown for migratory songbirds, but it is not well known how the simple genetic program encoding migratory distance and direction in young birds translates to a navigation mechanism used by adults. A number of convenient cues are available to define latitude on the basis of geomagnetic and celestial information, but very few are useful to defining longitude. To investigate the effects of displacements across longitudes on orientation, we recorded orientation of adult and juvenile migratory white-crowned sparrows, Zonotrichia leucophrys gambelii, after passive longitudinal displacements, by ship, of 266-2862 km across high-arctic North America. After eastward displacement to the magnetic North Pole and then across the 0 degrees declination line, adults and juveniles abruptly shifted their orientation from the migratory direction to a direction that would lead back to the breeding area or to the normal migratory route, suggesting that the birds began compensating for the displacement by using geomagnetic cues alone or together with solar cues. In contrast to predictions by a simple genetic migration program, our experiments suggest that both adults and juveniles possess a navigation system based on a combination of celestial and geomagnetic information, possibly declination, to correct for eastward longitudinal displacements.     

Polarized skylight does not calibrate the compass system of a migratory bat

In a recent study, Greif et al. (Greif et al. Nat Commun 5, 4488. (doi:10.1038/ncomms5488)) demonstrated a functional role of polarized light for a bat species confronted with a homing task. These non-migratory bats appeared to calibrate their magnetic compass by using polarized skylight at dusk, yet it is unknown if migratory bats also use these cues for calibration. During autumn migration, we equipped Nathusius'' bats, Pipistrellus nathusii, with radio transmitters and tested if experimental animals exposed during dusk to a 90° rotated band of polarized light would head in a different direction compared with control animals. After release, bats of both groups continued their journey in the same direction. This observation argues against the use of a polarization-calibrated magnetic compass by this migratory bat and questions that the ability of using polarized light for navigation is a consistent feature in bats. This finding matches with observations in some passerine birds that used polarized light for calibration of their magnetic compass before but not during migration.