Magnetoreception

The idea that animals perceive Earth’s magnetic field was once dismissed as impossible by physicists and biologists alike. Earth’s field is much too weak for an organism to detect, the argument went, and there are no possible biological mechanisms capable of converting magnetic-field information into electrical signals used by the nervous system.

Over time, however, evidence accumulated that animals do indeed perceive magnetic fields. It is now clear that diverse animals, ranging from invertebrates such as molluscs and insects to vertebrates such as sea turtles and birds, exploit information in Earth’s field to guide their movements over distances both large and small. What has remained mysterious is exactly how they do this.

Determining how the magnetic sense functions is an exciting frontier of sensory physiology. For sensory systems such as vision, hearing, and smell, the cells and structures involved in perceiving relevant sensory stimuli have been largely identified, and the basic way in which the sense operates is understood. In contrast, the cells that function as receptors for the magnetic sense have not been identified with certainty in any animal. Even the basic principles around which magnetic sensitivity is organized remain a matter of debate.

Earth’s magnetic field, also known as the geomagnetic field, provides animals with different sorts of information, which can be used for different purposes in navigation, as compasses and as maps. Sea turtles, salmon, and a few other animals use these magnetic cues to navigate during long-distance migrations. In the case of sea turtles, magnetic map information can be used either to guide a turtle toward a particular area or to help it assess its approximate location along a transoceanic migratory route. In effect, sea turtles have a low-resolution biological equivalent of a global positioning system, but one that is based on geomagnetic information instead of on satellite signals.

Experimental setup used in magnetic navigation experiments with sea turtles Hatchling loggerhead turtles were placed in a soft cloth harness and tethered in a circular pool of water surrounded by a magnetic coil system (boxlike structure), which could be used to reproduce the exact magnetic fields that exist in different parts of the ocean. Turtles swam in different directions when exposed to magnetic fields that exist at different locations along the migratory route, demonstrating that they can use Earth’s field to assess their geographic position in the ocean (Lohmann et al. 2001; Putman et al., 2011; Lohmann et al. 2012).

Searching for magnetoreceptors

Exactly how animals perceive magnetic fields is not known. There are several reasons why locating magnetoreceptors has proven to be unusually difficult. First, magnetic fields are unlike other sensory stimuli in that they pass unimpeded through biological tissue. Receptors for senses such as olfaction and vision must make contact with the external environment, but magnetoreceptors might plausibly be located almost anywhere inside an animal’s body. Second, magnetoreceptors might be tiny and dispersed throughout a large volume of tissue. Third, the transduction process might occur as a set of chemical reactions, in which case no obvious organ or structure devoted to this sensory system necessarily exists. If you imagine trying to find a small number of submicroscopic structures, possibly located inside cells scattered anywhere within an animal’s body, then you can begin to appreciate the challenge.

Several mechanisms have been proposed that might underlie magnetic-field detection. Most recent research, however, has focused on three main ideas: electromagnetic induction, magnetite, and chemical magnetoreception.

Electromagnetic induction

If a small bar composed of an electrically conductive material moves steadily through a magnetic field in any direction except parallel to the field lines, positively and negatively charged particles migrate to opposite sides of the bar. This results in a constant voltage, which in turn depends on the speed and direction of the bar’s motion relative to the magnetic field. If the moving bar is in a conductive medium that is stationary relative to the field, an electrical circuit is formed and current flows through the medium and the bar.

This same principle of electromagnetic induction might explain how elasmobranch fish (sharks, rays, and skates) perceive magnetism. The bodies of these animals are conductive. In addition, the fish have sensitive electroreceptors called ampullae of Lorenzini. These receptors are so sensitive to weak electrical changes that they might detect the voltage drop of induced currents that arise as the fish swim through Earth’s field. Whether elasmobranchs actually detect magnetic fields in this way, however, is not known.

Possible mechanism for a magnetic compass based on electromagnetic induction As a shark swims through Earth’s magnetic field, it induces weak electric currents to flow through the surrounding seawater. The induced current depends partly on the heading of the shark relative to the magnetic field. In effect, the shark uses its electric sense to infer its magnetic heading. (After Kalmijn 1978.)

Although using electromagnetic induction for magnetoreception may be plausible for elasmobranchs, it has two significant requirements: The animal must have sensitive electroreceptors, and the animal must live in an electrically conductive environment. Unlike water, air does not conduct electricity, so this mechanism appears unlikely for terrestrial animals. In addition, many aquatic animals such as sea turtles appear to lack electroreceptors, implying that another mechanism must be used.

Magnetite

A second hypothesis is that crystals of the mineral magnetite (Fe3O4) provide the physical basis for magnetoreception. The idea was inspired partly by the discovery that some bacteria produce magnetite crystals; as a result, the bacteria are physically rotated into alignment with magnetic field lines and can move along them. Magnetite has been detected in diverse animals known to perceive magnetic fields, but particularly detailed studies have been done with fish and birds.

In trout, magnetite has been found in the nose and appears to be closely associated with a nerve that responds to magnetic stimuli. Magnetite isolated from fish and other animals has mainly been in the form of single-domain crystals similar to those in bacteria. Single-domain crystals are tiny (about 50 nanometers [nm] in diameter), and each is a permanent magnet that will align with Earth’s magnetic field if permitted to rotate freely.

Such crystals might provide the basis for a magnetic sense in several different ways. For example, magnetite crystals might activate secondary receptors (such as hair cells, stretch receptors, or mechanoreceptors) as the particles try to align with the geomagnetic field. Alternatively, if magnetite crystals are located within cells and are connected to ion channels by cytoskeletal filaments, then the rotation of intracellular magnetite crystals might open ion channels directly, thus allowing ions to flow across the cell membrane to produce electrical signals used in communication by the brain and nervous system.

A hypothetical magnetite-based magnetoreceptor The green rectangle indicates a chain of single-domain magnetite crystals that forms a biological compass needle. The coils represent secondary receptors (stretch receptors) attached to the compass needle. The compass needle always attempts to rotate into alignment with Earth’s magnetic field but is constrained by the secondary receptors and has a limited range of motion. (1) When the animal is oriented in such a way that the compass needle is aligned toward the north, no force is exerted on either of the secondary receptors. (2) When the animal is oriented so that the compass needle is aligned in any other direction, one of the secondary receptors is stretched, eliciting action potentials, while the other is compressed. A few such receptor units, arranged orthogonally, could hypothetically provide the basis for a magnetic compass.

Chemical magnetoreception

Another hypothesis is that magnetoreception involves a set of unusual biochemical reactions that are influenced by Earth’s magnetic field. The hypothesized reactions involve pairs of free radicals (molecules with unpaired electrons) as fleeting intermediates. For this reason, the idea is sometimes called the radical pairs hypothesis.

The details of these chemical reactions are highly complex, but the putative process begins with an electron transfer from a donor molecule, A, to an acceptor molecule, B. This leaves each molecule with an unpaired electron; the two unpaired electrons have spins that are either opposite (singlet state) or parallel (triplet state). For a brief instant, the spin of each unpaired electron precesses, which means the axis of rotation changes in a way that can be likened to a spinning top wobbling around a vertical axis as it slows down. Precession of electron spins is caused by interactions with the local magnetic environment, which in turn depends on the combined magnetic fields generated by the spins and orbital motions of unpaired electrons and magnetic nuclei, plus the orientation and strength of any external field. Because the two unpaired electrons of molecules A and B encounter slightly different magnetic forces, they precess at different rates.

After a brief period of time, the electron that was transferred returns to the donor, a process known as backtransfer. Depending on the time that elapsed before backtransfer and the rates of precession for the two electrons, the original singlet or triplet state of the donor might be preserved or altered. For example, if backtransfer occurs quickly, then the electron spins will have precessed little and are likely to remain in their original opposite or parallel state, resulting in no change to molecules A and B. Alternatively, in a longer reaction, differences in the precession rates of the two unpaired electrons can change the original spin relationship, in which case A is chemically altered. This, in turn, can influence subsequent reactions or the chemical products that ultimately result. In sum, because an ambient magnetic field can influence the precession of electron spins under some circumstances, magnetic fields can influence some chemical reactions.

Where these reactions occur in animals, if indeed they do, is not known. An interesting clue, however, is that many of the best-known radical pair reactions begin with electron transfers that are induced by the absorption of light. This has led to the suggestion that chemical magnetoreceptors might also be photoreceptors. Recent attention has focused on cryptochromes, which are blue-sensitive photoreceptive proteins known to exist in numerous animals. Some researchers think that cryptochromes have the right chemical properties to function as magnetoreceptors.

The most direct evidence for cryptochrome involvement has come from experiments with the fruit fly Drosophila, in which flies were trained to enter one arm of a simple maze on the basis of magnetic-field conditions. Mutant flies lacking genes for cryptochrome were unable to perform this task, but magnetic sensitivity was restored when cryptochrome genes were inserted into the flies. Further research will be needed to determine whether the principles discovered in flies are applicable to other organisms.

References

Gegear, R. J., A. Casselman, S. Waddell, and S. M. Reppert. 2009. Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature 454: 1014–1018.

Johnsen, S., and K. J. Lohmann. 2005. The physics and neurobiology of magnetoreception. Nat. Rev. Neurosci. 6: 703–712.

Johnsen, S., and K. J. Lohmann. 2008. Magnetoreception in animals. Physics Today 61: 29–35.

Kalmijn, A. J. 1978. Experimental evidence of geomagnetic orientation in elasmobranch fishes. In K. Schmidt-Koenig and W. T. Keeton (eds.), Animal Migration, Navigation, and Homing, pp. 347–353. Springer, Berlin.

Lohmann, K. J., S. D. Cain, S. A. Dodge, and C. M. F. Lohmann. 2001. Regional magnetic fields as navigational markers for sea turtles. Science. 294: 364–366.

Lohmann, K. J., C. M. F. Lohmann, and N. F. Putman. 2007. Magnetic maps in animals: nature’s GPS. J. Exp. Biol. 210: 3697–3705.

Lohmann, K. J., N. F. Putman, and C. M. F. Lohmann. 2011. The magnetic map of hatchling loggerhead sea turtles. Curr. Opin. Neurobiol. 22: 336–342.

Putman, N. F., C. S. Endres, C. M. F. Lohmann, and K. J. Lohmann. 2011. Longitude perception and bicoordinate magnetic maps in sea turtles. Curr. Biol. 21: 463–466.

Rodgers, C. T., and P. J. Hore. 2009. Chemical magnetoreception in birds: the radical pair mechanism. Proc. Natl. Acad. Sci. U.S.A. 106: 353–360.

Wiltschko, R., and W. Wiltschko. 2006. Magnetoreception. BioEssays 28: 57–168.

Wiltschko, W., and R. Wiltschko. 2005. Magnetic orientation and magnetoreception in birds and other animals. J. Comp. Physiol., A 191: 675–693.

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