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Author(s) of the publication: Gennady SHVETSOV

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by Gennady SHVETSOV, Cand. Sc. (Biol.), Head of the Section on Problems of Biological Navigation, RADUGA State R&D Center of the Russian Federation (town of Raduzhny, Vladimir Region)

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Articles in this rubric reflect the opinion of the author.-Ey.

The problem of space orientation of animals-the mechanism of navigation and homing in more common terms-has been in the focus of attention at least ever since the time of Aristotle. Migration is best known among birds which periodically travel from north to south and back over vast distances. And the really amazing thing is, as proved by the results of experiments with the ringing of birds' legs, migratory birds usually return to their original, or native, breeding grounds.

The polar gull (Sterna paradisaea), for example, covers a distance of 60 thousand kilometers one way from the Arctic isles to the cliffs of Antarctica which takes it nearly three months one way. The golden plover (Charadrius apricarius) flies non- stop over the Pacific from Alaska to the Hawaiis for some 40 hours, rain or shine, covering a distance of three and a half thousand kilometers. This seems to be the record performance of this kind known to ornithologists today. To add color to the drama one also has to bear in mind that as often as not such overflights occur even despite the odds of heavy clouds and/or thick fog (blind flying) without even the slightest chance of sighting any visible landmarks on earth or up in heaven.

Or take the example of cuckoo fledglings which, brought up by foster parents, can fly all by themselves to the tropics over thousands of kilometers landing exactly in their traditional wintering grounds where they mix with birds of the feather from other places. A similar situation is observed with young starlings (with the only difference that they now fly to their wintering grounds earlier than their forefathers).

Or take another example-of the North American monarch or milkweed butterflies (Danaidae) which fly 4,000 km to the south before they start to breed and multiply over and over again. And that means that the butterflies which come back later are several generations younger than their parents and even grandparents.

Studies of various modes of migration of birds, butterflies, bees, frogs, and so on lead us to the conclusion that all of these creatures must know exactly their summer and winter "homes" and also have a reliable all-weather biological compass which keeps them on course with an accuracy of fractions of a degree. Leaving aside the "address data" of various species for the time being, let us first take a closer look at the mechanism of navigation and homing, or orientation.

One of the hypotheses on that score pins on the effect of the Earth's magnetic field. This seems to be supported by the fact that the bodies of various representatives of the fauna contain magnetic particles of biological origin (grains of biogenic magnetite). These were found by American researchers (D. Gold, 1978) in worker bees, carrier (homing) pigeons (B. Walcot, 1979), monarch (milkweed) butterflies (B. McFalden, D. Jones, 1982), sea turtles (E. Perry, 1982), etc. Assuming that the Earth's magnetic field brings these particles into some order, the nervous system of an animal should be able to detect these patterns as the basis of what one can call "compass sense". But for this mechanism to work a living being should have within its body from 105 to 106 such grains-something that does not happen in reality.

This fact rebuts the above theory as has been proved by numerous direct experiments. In one such experiment researchers attached to the backs of homing pigeons magnet strips which caused a magnetic field disturbance around the bird. But the pigeons, both with and without magnets, had no problems finding their way to their lofts. And there is yet another external factor which buries the above doctrine. The magnetic field of the Earth is rather variable in space with the declination range from 40 East (North America) to 60 West (Greenland). And only upon the zero value lines of this parameter-of which there are but two on the globe-the compass needle points exactly to the North. What is more, terrestrial magnetic field parameters are subject to time variations with what we call daily, monthly and annual fluctuations, to

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say nothing of frequent magnetic storms (because of which our magnetic maps have to be updated every 5 to 10 years).

And there were also other hypotheses for the mechanism of space orientation or compass sense of animals (such as "inertial" one, by visible landmarks, by infrared radiation, astronomical, etc.). None of these, however, offers any reliable clues to the mechanisms of the process of migration, solo or in flocks, and over practically any distances. And this failure is due to the obvious fact that all of these theories rely on "reference points" which fluctuate in space and time, are often unpredictable and prone to distortions. Having said that, what does happen in reality?

As for the author of this article, he has been doing his honest best to steer clear of the errors of his predecessors in his basic assumptions and then in his calculations and experiments. To begin with, he singled out and analyzed the invariable characteristics of properties of near-Earth environment which can serve as "sure-fire" bearings for migratory birds, insects or what have you. Later on he was able to pinpoint the "biological compass" which not only detects the exact position of a "migrant" at any given time, but traces its position all through the process of migration and the exact homing on its final destination. This "navigation aid" has been thoroughly investigated and attempts are under way to translate this mechanism into industrial reality. But let us consider one thing at a time.

Any material bodies, biological objects including, are subjected to only two constant forces in each and every point of near-earth space or environment. Their strength and direction are independent from the season, weather conditions or any other factors because this is the gravitational pull of the Earth (centripetal), and the force of the planet's rotation from west to east. The former gradually grows from the equator to the poles, and the latter-the other way round. What is more, the linear rotation velocity in any point depends on its distance from the Earth (the greater is the radius of rotation, the greater is its value). And one more thing. The above forces are of different physical nature and thus cannot be superimposed; and so they are picked by animals separately, one by one. And now let us try and visualize the flight of a bird under the effect of the above factors.

Flapping their wings, birds progress in a certain direction and overcome the gravitational pull of the Earth. Their center of gravity moving up and down, it would seem that their flight trajectory should be sinusoidal. In fact, this is not so because, apart from the above two movements, a bird is also involved in a third one which is the momentum of rotation of the planet. Thanks to that and depending on their distance from the ground, birds in flight deviate to different degrees of magnitude along the east-west line.

If we take as the reference point a "middle position" (with the wings parallel to the ground), the bird will be seen to oscillate from it in the

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horizontal plane (west-east or east-west). There oscillations are of a periodic nature and are displaced with respect to the vertical shifts in a way that the maximum of one matches the zero value of the other. And so on. Putting together all of these three movements in which the flying bird is involved at one and the same time, one discovers that the flight trajectory assumes the form of a spiral, stretched in a vertical direction.

So, the "physics" of a bird's flight can be visualized well enough so as to determine the time-invariable characteristics which "actuate" the avian biological compass. These, as has been said, include the gravitational pull and inertia, the latter determining the linear velocity of movement in any point of space. And now let us take a closer look at the mysterious biological compass and see how the flying migrants determine their position in some concrete point in time and guide their progress.

Any guidance device used for orientation starts to operate and points in the right direction if it is placed in a strictly horizontal position-on a stabilized support. With birds this function is performed by the head. Located within it (in the inner ear) is the vestibular apparatus-the space analyzer which guides the directional flight.

It consists of three what are called semi-circular and mutually perpendicular channels (front, rear and horizontal) which are tubular in shape and filled with a special fluid- endolymph. And there are also two twin (left and right) formations: an oval sac- utriculus (utricle) and a spherical one-sacculus. All of these things taken together are miniature gravitational- inertial sensors. They are based on fiber-like receptor cells sensitive to external forces and their slightest variations. Part of the inner surface of the utriculus and sacculus (where the receptor cells are located) is covered with elastic epithelium. In the first it is located horizontally and in the second-vertically. Close to the epithelium there kind of floats a gel-like membrane filled with a multitude of fine lime stones-otoliths and covering the ends of the receptor fibers. The remaining space is filled with endolymph whose density is three times less than of the otoliths. That is why when a bird accelerates its flight the otolith membrane lags behind the movement of the endolymph from inertia causing the fibers to bend. When their tips move only by 10'10 to 10"11 m, the cells begin to respond by generating an electric signal supplied to an appropriate neuron of the brain.

And one should note one important feature. The top of the fiber bunch of each cell- kinocilium-is oriented in space in a certain way (morphologically polarized). And when the direction of a stimulating signal (inertia opposite to acceleration) coincides with the orientation of the kinocilium, the receptor generates the maximal signal. If there is some angle between them, the response of the fibers diminishes and fades away altogether at an angle of 90*.

During the self-orientation of a bird in space the functions of the

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utriculus and sacculus are strictly separated: the first controlling its position and flight direction in the horizontal plane and the second measuring the latitude. At the same time during the entire flight they help keep the head of the bird in a strictly horizontal position, turning it into a kind of a stabilizing platform of the biological compass.

The mechanical momentum is transmitted in a somewhat different way to the kinocilia in the semicircular canals. In each of them there is an expanded section, the ampulla. Positioned across it, like a membrane, is a layer of elastic tissue covered with a gell-like cupule into which the bunches of receptor fibers are immersed. During angular acceleration, as soon as the bird moves its head up or down or turns it, the endolymph lags behind from inertia and exerts pressure on the cupule which in its turn acts upon the kinocilium and bends it. As a result a corresponding signal is transmitted to the brain which restores the head in its original position.

Now what about the role of the biological compass in space orientation and flight direction? As has been said already, the utriculus is oval-shaped, and the Likewise shaped otolith membrane and sensor matrix are located on the horizontal plane. The latter consists of a large number of capillary (hair) cells located not chaotically, but in a radial manner all around the circle. Their "radii" are so close to one another that the angles between them measure but few seconds only. The morphologically polarized cell kinocilia are located along them, but only those of them are triggered at a certain moment which coincide with the direction of the reverse "east-west" oscillations of the bird. And since the biocompass is actuated with the first flap of the

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wings, the bird is constantly aware in a precise way of the direction of its flight being able to correct it if need be. At the same time the sac-culus senses the slightest changes of the gravitational pull (which depends on the latitude) and when the bird reaches its "destination", it gives the signal for landing.

So how do migratory birds know at which azimuth they should take off and at what latitude they should land? Numerous observations by ornithologists and their experiments lead us to the conclusion that all the necessary data are stored genetically. One interesting experiment bearing out this conclusion was staged in the following way: some kinds of birds were taken in cages a long distance away from their nests (several time belts away) whereupon they were released. In the process of the subsequent migration they took off at exactly the same azimuth as the control samples at their nesting grounds. What is more, the former and the latter landed at one and the same latitude, but at a distance equal to their original takeoff position.

Specialists also noted that before taking off birds fly three incomplete circles around their nests within a radius of 150-200 m before they set on their course, so to say. These circles are no "farewell" ritual as some people thought, but are a "warming up" procedure for all the radii of the utriculus at which the capillary or hair cells are located. In this way the "west-east" orientation is asserted. The kinocilium then generates the strongest signal thus "fixing" the flight azimuth at a given moment of time. Coincidence with the genetic "code" determines the original direction of the flight. The first two circles are "test runs" and the flight begins from the third one. After that no matter what the conditions may be, bad weather or spending the night off the "main course" of flight-the steadily working biocompass will always point in the right direction.

Summing it up, the author is offering a hypothesis of the mechanism of what we call autonomous orientation and navigation of birds (and all vertebrates). The sensitivity of the biocompass is directlydependent on the mass of the otolithic membrane of the utriculus and inversely dependent on the rigidity of its suspension. The angular resolution of this self-governing "device" depends on the number of sensor capillary cells whose axes are extremely sensitive and are located in the radial directions all around the circumference. The flight program for migrating birds is input during the circular flight around their nest and the flight coordinates are controlled by the central nervous system with the help of the sacculus and the utriculus which analyze the gravitational pull and the flight azimuth at any given moment of time.



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