Integrated use of moon and magnetic compasses by the heart-and-dart moth,Agrotis exclamationis

Use of the moon as a compass during migration appears difficult due to the complexity of the moon's change in azimuth during the lunar month. These apparent difficulties would be eased if the moon's position were calibrated at intervals against a constant reference source, such as the geomagnetic field. Yet, until now, no animal has been shown to integrate moon and magnetic compasses for orientation. In this study, light-traps were used on 15 nights during a lunar month to obtain samples of heart-and-dart moths, Agrotis exclamationis, characterized by a preference to fly ‘toward’ (i.e.±90°) the moon's azimuth. The compass orientation of each sample was then tested in normal and reversed geomagnetic fields, out of sight of the moon. Compass orientation relative to the ambient magnetic field coincided with the compass bearing of the moon at the time of capture. Directional preference changed during the lunar month in a way that tracked the change in the moon's azimuth. It is concluded that moths use the geomagnetic field to calibrate a moon compass.     

Moonlight and the Migratory Orientation of Savannah Sparrows (Passerculus sandwichensis)

Migratory birds might respond to moonlight in at least four ways: (1) a geographical reference for selecting a compass direction, (2) a celestial ‘landmark’ to facilitate maintenance of a preferred heading, (3) a stimulus that distracts migrants and introduces error in compass orientation, or (4) a source of illumination that facilitates nocturnal flight. This study examines the response of migratory savannah sparrows (Passerculus sandwichensis) to moonlight during controlled tests in orientation cages. I found no evidence that savannah sparrows use a lunar compass to select a direction. If savannah sparrows do use the moon as a ‘landmark’ to maintain a direction selected with reference to a different cue, I expected birds to be better oriented on overcast nights when the moon is present than they are when the moon is absent. The results suggest otherwise. Usually, savannah sparrows respond phototactically to the moon by directing their cage activity toward or at a constant angle with respect to the moon's azimuth. Interestingly, the migrant's response to moonlight depended on whether the bird viewed the setting sun earlier that evening.     

Nocturnal orientation by the Asian honey bee, Apis dorsata

Honey bees have been observed to forage and dance on moonlit nights, but it has never been established whether the moon serves as a reference in orienting nocturnally active bees. The present study, of the Asian honey bee Apis dorsata, suggests that although the moon's illumination is essential for nocturnal flight, the moon itself is ignored for orienting the dances. Rather, bees probably use the sun's position as a reference point for their dances, even though the sun is below the horizon. This ability may involve an extension of the mechanism that honey bees employ to find the sun on overcast days.     

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.     

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.     

Pineal Body and Magnetic Sensitivity: Homing in Pinealectomized Pigeons under Overcast Skies

Since birds use the earth's magnetic field for compass orientation when astronomical cues are lacking and it has recently been suggested that the pineal body is part of their magnetic compass, test releases have been performed in overcast conditions with pigeons deprived of the pineal body. On the whole, both experimental and control birds were capable of homeward orientation, though the bearings of experimental were rather more scattered. No differences in homing speed or success were recorded. Thus, the pineal body does not appear to play an important role in the homing of pigeons.     

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.     

Dung beetles ignore landmarks for straight-line orientation

Upon locating a suitable dung pile, ball-rolling dung beetles shape a piece of dung into a ball and roll it away in a straight line. This guarantees that they will not return to the dung pile, where they risk having their ball stolen by other beetles. Dung beetles are known to use celestial compass cues such as the sun, the moon and the pattern of polarised light formed around these light sources to roll their balls of dung along straight paths. Here, we investigate whether terrestrial landmarks have any influence on straight-line orientation in dung beetles. We find that the removal or re-arrangement of landmarks has no effect on the beetle’s orientation precision. Celestial compass cues dominate straight-line orientation in dung beetles so strongly that, under heavily overcast conditions or when prevented from seeing the sky, the beetles can no longer orient along straight paths. To our knowledge, this is the only animal with a visual compass system that ignores the extra orientation precision that landmarks can offer.     

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.     

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

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

Orientation in pied flycatchers: the relative importance of magnetic and visual information at dusk

We investigated the orientation of juvenile pied flycatchers, Ficedula hypoleuca, during autumn migration in south Sweden using orientation cage experiments, to study the relative importance of visual and magnetic information at sunset. We performed cage tests under 12 experimental conditions that manipulated the geomagnetic and visual sunset cues available for orientation: natural clear skies in the local or a vertical magnetic field; simulated total overcast in the local or a vertical magnetic field; natural pattern of skylight polarization and directional information from stars screened off, with the sun's position as normal or shifted 120 degrees anticlockwise with mirrors; reduced polarization in the local or a vertical magnetic field; directions of polarization (e-vector) NE/SW and NW/SE, respectively, in the local or a vertical magnetic field. The pied flycatchers were significantly oriented towards slightly south of west when they could use a combination of skylight and geomagnetic cues. The mean orientation was significantly shifted along with the deflection of the sunset position by mirrors. Reduced polarization had no significant effect on orientation either in the local, or in a vertical, magnetic field. The birds tended to orient parallel with the axis of polarization, but only when the artificial e-vector was aligned NW/SE. The mean orientation under simulated total overcast in a vertical, and in the local, magnetic field was not significantly different from random. It is difficult to rank either cue as dominant over the other and we conclude that both visual and magnetic cues seem to be important for the birds' orientation when caught and tested during active migration. Copyright 1999 The Association for the Study of Animal Behaviour.     

Solar cues in the migratory orientation of the Savannah sparrow, Passerculus sandwichensis

Results clearly implicate the setting sun as a critical source of directional information in the migratory orientation of the savannah sparrow, Passerculus sandwichensis. Savannah sparrows allowed a view of both sunset and stars displayed oriented behaviour in biologically meaningful directions during spring and fall seasons. When the same individuals were denied a view of sunset, and tested under the stars alone, disorientation characterized their behaviour. Furthermore, birds allowed a view of sunset, but tested under ‘overcast’ night skies (no stars visible), displayed well-oriented behaviour indicating the sufficiency of sunset. Experiments in which the migrant's internal chronometer was shifted suggested a fixed-angle (menotactic) response to the sunset cue rather than a time-compensating compass mechanism. I believe stars are valuable to this migrant as celestial reference points. Orientational information gained at the time of sunset is transferred to stars on a nightly basis. The relationship between solar and stellar cues is apparently hierarchical in the savannah sparrow. Information necessary to select the appropriate migratory direction is gained from the primary cue, the setting sun, while maintenance of that heading is dependent on a secondary cue, probably the stars.     

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.     

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.     

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 .     

Moon and sun compasses in sandhoppers rely on two separate chronometric mechanisms

The relationship between the chronometric system of compensation for the apparent movement of the sun and that for the moon has been the subject of several, never proven, hypotheses. Our studies on sandhoppers have demonstrated that the chronometric mechanism of the moon compass is separate from that of the sun compass. They show (i) that a period of seven days in constant darkness has no influence on the capacity for orientation, either solar or lunar, and indicates the presence of one or more continuously operating timing mechanisms; (ii) that two different shifts in the light–dark phase have no effect on the chronometric mechanism of lunar orientation, but they do affect that of solar orientation; and (iii) that exposure to an artificial moon delayed by seven days with respect to the natural cycle causes the expected change in the mean direction of individuals tested under the natural moon, but not of those tested under the sun.     

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.

     

Orientation at night: an innate moon compass in sandhoppers (Amphipoda: Talitridae)

The supralittoral amphipod Talitrus saltator is well known for its capacity for astronomical orientation using the sun and moon as compasses. It has also been demonstrated that the sun compass is innate in this species. In our experiments, we released inexpert (naive) young born in the laboratory into a confined environment under the full moon and in the absence of the horizontal component of the magnetic field. They were allowed to see the natural sky and the moon only at the moment of release. The young individuals were obtained in the laboratory by crossing adult individuals from the same and different populations of sandhoppers. The young from intrapopulation crosses were well oriented towards the directions corresponding to those of their parents, whereas the young from interpopulation crosses were oriented in an intermediate direction. Therefore, our experiments demonstrate in the sandhopper T. saltator that sea-land moon orientation relies on an innate chronometrically compensated mechanism.     

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.     

Magnetic induction for the sensing of magnetic fields by animals—An analysis

Magnetic induction is analyzed as a possible mechanism for the detection of weak magnetic fields by animals. The range of parameters possible for a system which provides a signal greater than thermal noise and meets other constraints is determined. It is concluded that an organ millimeters in size is required to sense the Earth's field by induction. The labyrinth of the inner ear is discussed in these terms.