Question: How many species use magnetoreception?

Magnetoreception


Magnetoreception (also magnetoception) is a sense which allows an organism to detect a magnetic field to perceive direction, altitude or location. This sensory modality is used by a range of animals for orientation and navigation,[1] and as a method for animals to develop regional maps. For the purpose of navigation, magnetoreception deals with the detection of the Earth's magnetic field.
Magnetoreception is present in bacteria, arthropods, molluscs and members of all major taxonomic groups of vertebrates.[1] Humans are not thought to have a magnetic sense, but there is a protein (a cryptochrome) in the eye which could serve this function.[2]
Proposed mechanisms
Magnetotactic Bacteria
Magnetotactic bacteria is a class of bacteria known to use magnetic fields for orientation. These bacteria demonstrate a behavioral phenomenon known as magnetotaxis which is how the bacterium orients itself and migrates in the direction along the Earth's magnetic field lines. The bacteria contain magnetosomes, which are nanometer-sized particles of magnetite or iron sulfide enclosed within the bacterial cells.[3] The magnetosomes are surrounded by a membrane composed of phospholipids and fatty acids and contain at least 20 different proteins.[4]  Magnetosomes form in chains where the magnetic moments of each magnetosome align in parallel, causing each bacterium cell to essentially act as a magnetic dipole, giving the bacteria their permanent-magnet characteristics.
Cryptochromes
For animals the mechanism for magnetoreception is unknown, but there exist two main hypotheses to explain the phenomenon.[5]
According to one model, magnetoreception is possible via the radical pair mechanism.[6] The radical-pair mechanism is well-established in spin chemistry,[7][8][9] and was speculated to apply to magnetoreception in 1978 by Schulten et al.. In 2000, cryptochrome was proposed as the "magnetic molecule", so to speak, that could harbor magnetically sensitive radical-pairs. Cryptochrome, a flavoprotein found in the eyes of European robins and other animal species, is the only protein known to form photoinduced radical-pairs in animals.[6]  The function of cryptochrome is diverse across species, however, the photoinduction of radical-pairs occurs by exposure to blue light, which excites an electron in a chromophore.[10]  The Earth's magnetic field is only 0.5 gauss and so it is difficult to conceive of a mechanism, other than phase shift, by which such a field could lead to any chemical changes other than those affecting the weak magnetic fields between radical pairs.[11] Cryptochromes are therefore thought to be essential for the light-dependent ability of the fruit fly Drosophila melanogaster to sense magnetic fields.[12]
Iron Based
The second proposed model for magnetoreception relies on clusters composed of iron, a natural mineral with strong magnetism. The idea is favorable as it builds up on the magnetoreceptive abilities of magnetotactic bacteria. These iron clusters have been observed mainly in homing pigeons in the upper beak,[13] but also in other taxa[14].
These iron clusters have been observed in two types of compounds: magnetite (Fe3O4) and maghemite (γ-Fe2O3). Both are believed to play a part in the magnetic sense, particularly for the magnetic map sense[15][16]. These concentrations are believed to be connected to the central nervous system to form a sensing system. Research has focused on magnetite concentrations, however, magnetite alone has been shown to not be in magnetosensitive neurons.[17]
Maghemite has been observed in platelets concentrated along the dendrites of the upper beak, consistently in the nanoscale. When in the nanoscale, iron oxides will remain permanently magnetized at lengths greater than 50 nm and will become magnetized at lengths smaller than 50 nm.[18] Since these platelets have been observed in collections of 5-10, they are thought to form dipoles local to the dendrite they are present in. These local magnetic changes then cause a mechanical response along the membrane of the nerve cell, leading to a change in ion concentrations. This ion concentration, with respect to the other dendrite clusters is believed to form the magnetic sense[16].
Ampullae of Lorenzini
Another less general type of magnetic sensing mechanism in animals that has been described is electromagnetic induction used by sharks, stingrays and chimaeras (cartilaginous fish).  These species possess a unique electroreceptive organ known as ampullae of Lorenzini which can detect a slight variation in electric potential.  These organs are made up of mucus-filled canals that connect from the skin's pores to small sacs within the animal's flesh that are also filled with mucus.  The ampullae of Lorenzini are capable of detecting DC currents and have been proposed to be used in the sensing of the weak electric fields of prey and predators. These organs could also possibly sense magnetic fields, by means of Faraday's law: as a conductor moves through a magnetic field an electric potential is generated. In this case the conductor is the animal moving through a magnetic field, and the potential induced depends on the time varying rate of flux through the conductor according to





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These organs detect very small fluctuations in the potential difference between the pore and the base of the electroreceptor sack. An increase in potential results in a decrease in the rate of nerve activity, and a decrease in potential results in an increase in the rate of nerve activity. This is analogous to the behavior of a current carrying conductor; with a fixed channel resistance, an increase in potential would decrease the amount of current detected, and vice versa. These receptors are located along the mouth and nose of sharks and stingrays.[19][20] Although debated, it has been proposed that in terrestrial animals the semicircular canals of the inner ear could host a magnetosensitive system based on electromagnetic induction.[21]
In invertebrates and fish
The nematode Caenorhabditis elegans was proposed to orient to the magnetic field of the Earth using the first described set of magnetosensory neurons.[22] Worms appear to use the magnetic field to orient during vertical soil migrations that change in sign depending on their satiation state (with hungry worms burrowing down, and satiated worms burrowing up). However, recent evidence challenges these findings. [23][24]
The mollusk Tochuina tetraquetra (formerly Tritonia diomedea or Tritonia gigantea) has been studied for clues as to the neural mechanism behind magnetoreception in a species. Some of the earliest work with Tochuina showed that prior to a full moon Tochuina would orient their bodies between magnetic north and east.[25] A Y-maze was established with a right turn equal to geomagnetic south and a left turn equal to geomagnetic east. Within this geomagnetic field 80% of Tochuina made a turn to the left or magnetic east. However, when a reversed magnetic field was applied that rotated magnetic north 180° there was no significant preference for either turn, which now corresponded with magnetic north and magnetic west. These results, though interesting, do not conclusively establish that Tochuina uses magnetic fields in magnetoreception. These experiments do not include a control for the activation of the Rubens’ coil in the reversed magnetic field experiments. Therefore, it is possible that heat or noise generated by the coil was responsible for the loss of choice preference.  Further work with Tochuina was unable to identify any neurons that showed rapid changes in firing as a result of magnetic fields.[26][27] However, pedal 5 neurons, two bisymmetric neurons located within the Tochuina pedal ganglion, exhibited gradual changes in firing over time following 30 minutes of magnetic stimulation provided by a Rubens’ coil.  Further studies showed that pedal 7 neurons in the pedal ganglion were inhibited when exposed to magnetic fields over the course of 30 minutes. The function of both pedal 5 neurons and pedal 7 neurons is currently unknown.

Drosophila melanogaster is another invertebrate which may be able to orient to magnetic fields. Experimental techniques such as gene knockouts have allowed a closer examination of possible magnetoreception in these fruit flies. Various Drosophila strains have been trained to respond to magnetic fields.[12] In a choice test flies were loaded into an apparatus with two arms that were surrounded by electric coils. Current was run through each of the coils, but only one was configured to produce a 5-Gauss magnetic field at a time. The flies in this T-maze were tested on their native ability to recognize the presence of the magnetic field in an arm and on their response following training where the magnetic field was paired with a sucrose reward. Many of the strains of flies showed a learned preference for the magnetic field following training. However, when the only cryptochrome found in Drosophila, type 1 Cry, is altered, either through a missense mutation or replacement of the Cry gene, the flies exhibit a loss of magnetosensitivity. Furthermore, when light is filtered to only allow wavelengths greater than 420nm through, Drosophila loses its trained response to magnetic fields. This response to filtered light is likely linked to the action spectrum of fly-cryptochrome which has a range from 350nm – 400nm and plateaus from 430-450nm.[28]   Although researchers had believed that a tryptophan triad in cryptochrome was responsible for the free radicals on which magnetic fields could act, recent work with Drosophila has shown that tryptophan might not be behind cryptochrome dependent magnetoreception. Alteration of the tryptophan protein does not result in the loss of magnetosensitivity of a fly expressing either type 1 Cry or the cryptochrome found in vertebrates, type 2 Cry.[29] Therefore, it remains unclear exactly how cryptochrome mediates magnetoreception. These experiments used a 5 gauss magnetic field, 10 times the strength of the Earth's magnetic field). Drosophila has not been shown to be able to respond to the Earth’s weaker magnetic field.
Studies of magnetoreception in vertebrate fish have been conducted mainly with salmon. For instance, the presence of an internal magnetic compass has been discovered in Sockeye Salmon (Oncorhynchus nerka).[30] Researchers made this discovery by first placing the young of this species in a symmetrical, circular tank and allowing them to pass through exits in the tank freely. A mean vector was then calculated to represent the directional preferences of these salmon in the natural magnetic field. Notably, when the magnetic field was experimentally rotated, the directional preferences of the young Sockeye Salmon changed accordingly.[30] As such, researchers concluded that the orientation of swimming behaviour in Sockeye Salmon is influenced by magnetic field information.
Further research regarding magnetoreception in salmon has investigated Chinook Salmon (Oncorhynchus tschawytscha). To induce a preference for magnetic East-West, a group of these salmon were housed in a rectangular tank with water flowing from west to east for eighteen months.[31] This group was also fed exclusively at the west end of the tank during this period. Upon placing these same salmon in a circular tank with symmetrical water flow, a preference for aligning their bodies with magnetic East-West was observed as expected. However, when the magnetic field was rotated by 90°, the salmon changed their preferred orientation to the North-South axis.[31] From these results, researchers concluded that Chinook Salmon have the capacity to use magnetic field information in directional orientation.
Magnetoreception is well documented in honey bees, ants and termites.[32]  In ants and bees, this is used to orient and navigate in areas around their nests and within their migratory paths.[33] For example, through the use of magnetoreception, the Brazilian stingless bee Schwarziana quadripunctata is able to distinguish differences in altitude, location, and directionality using the thousands of hair-like particles on its antennae.[34]
Magnetoreception has also been reported in the European eel by at least one study.[35]
In amphibians and reptiles
A number of amphibians and reptiles including salamanders, toads and turtles exhibit alignment behaviours with respect to the Earth's magnetic field.
Some of the earliest studies of amphibian magnetoreception were conducted with cave salamanders (Eurycea lucifuga). Researchers housed groups of cave salamanders in corridors aligned with either magnetic North-South, or magnetic East-West. In ensuing tests, the magnetic field was experimentally rotated by 90°, and salamanders were placed in cross-shaped structures (one corridor along the new North-South axis, one along the new East-West axis).[36] Considering these salamanders showed a significant preference for test corridors which matched the magnetic alignment of their housing corridors, researchers concluded that cave salamanders have the capacity to detect the Earth’s magnetic field, and have a preference for movement along learned magnetic axes.[36]
Subsequent research has examined magnetoreception in a more natural setting. Under typical circumstances, red-spotted newts (Notophthalmus viridescens) respond to drastic increases in water temperature (which tend to indicate environmental deterioration) by orienting themselves toward the shoreline and heading for land.[37] However, when magnetic fields are experimentally altered, this behaviour is disrupted, and assumed orientations fail to direct the newts to the shoreline.[37] Moreover, the change in orientation corresponds to the degree by which the magnetic field is shifted.[37] In other words, inversion of the magnetic poles (a 180° shift) results in inversion of the typical orientation (a 180° shift). Further research has shown that magnetic information is not only used by red-spotted newts for orientation toward the shoreline, but also in orientation toward their home pools.[38] Ultimately, it seems as though red-spotted newts rely on information regarding the Earth’s magnetic field for navigation within their environment, in particular when orienting toward the shoreline or toward home.[37]
In similar fashion, European (Bufo bufo) and Natterjack (Epidalea calamita) toads appear to rely, at least somewhat, on magnetic information for certain orienting behaviours. These species of anurans are known to rely on vision and olfaction when locating and migrating to breeding sites, but it seems magnetic fields may also play a role. When randomly displaced from their breeding sites, these toads remain well-oriented, and are capable of navigating their way back, even when displaced by more than 150 meters.[39] However, when this displacement is accompanied by the experimental attachment of small magnetic bars, toads fail to relocate breeding sites.[40] Considering experimental attachment of non-magnetized bars of equal size and weight does not affect relocation, it seems that magnetism is responsible for the observed disorientation of these toads.[40] Therefore, researchers have concluded that orientation toward breeding sites in these anurans is influenced by magnetic field information.[41]

The majority of study on magnetoreception in reptiles involves turtles. Some of the earliest support for magnetoreception in turtles was found in Terrapene carolina, a species of box turtle. After successfully teaching a group of these box turtles to swim to either the east or west end of an experimental tank, the introduction of a strong magnet into the tank was enough to disrupt the learned routes.[42] As such, the learning of oriented paths seems to rely on some internal magnetic compass possessed by box turtles. Subsequent discovery of magnetite in the dura mater of Sea Turtle hatchlings supported this conclusion, as magnetite provides a means by which magnetic fields may be perceived.[43]
Furthermore, orientation toward the sea, a behaviour commonly seen in hatchlings of a number of turtle species, may rely, in part, on magnetoreception. In Loggerhead and Leatherback turtles, breeding takes place on beaches, and, after hatching, offspring crawl rapidly to the sea. Although differences in light density seem to drive this behaviour, magnetic alignment may also play a part. For instance, the natural directional preferences held by these hatchlings (which lead them from beaches to the sea) reverse upon experimental inversion of the magnetic poles, suggesting the Earth’s magnetic field serves as a reference for proper orientation.[44]
In homing pigeons
Homing pigeons can use magnetic fields as part of their complex navigation system.[45] William Keeton showed that time-shifted homing pigeons are unable to orient themselves correctly on a clear, sunny day which is attributed to time-shifted pigeons being unable to compensate accurately for the movement of the sun during the day. Conversely, time-shifted pigeons released on overcast days navigate correctly. This led to the hypothesis that under particular conditions, homing pigeons rely on magnetic fields to orient themselves. Further experiments with magnets attached to the backs of homing pigeons demonstrated that disruption of the bird's ability to sense the Earth's magnetic field leads to a loss of proper orientation behavior under overcast conditions.[46] There have been two mechanisms implicated in homing pigeon magnetoreception: the visually mediated free-radical pair mechanism and a magnetite based directional compass or inclination compass.[47]  More recent behavioral tests have shown that pigeons are able to detect magnetic anomalies of 186 microtesla (1.86 Gauss).[48]
In a choice test birds were trained to jump onto a platform on one end of a tunnel if there was no magnetic field present and to jump onto a platform on the other end of the tunnel if a magnetic field was present. In this test, birds were rewarded with a food prize and punished with a time penalty. Homing pigeons were able to make the correct choice 55%-65% of the time which is higher than what would be expected if the pigeons were simply guessing. 
For a long time the trigeminal system was the suggested location for a magnetite-based magnetoreceptor in the pigeon. This was based on two findings: First, magnetite-containing cells were reported in specific locations in the upper beak.[49] Subsequent studies, however, revealed that these cells were macrophages, not magnetosensitive neurons.[50] [51] Second, pigeon magnetic field detection is impaired by sectioning the trigeminal nerve and by application of lidocaine, an anesthetic, to the olfactory mucosa.[52] However, lidocaine treatment might lead to unspecific effects and not represent a direct interference with potential magnetoreceptors.[53]  Therefore, an involvment of the trigeminal system is still debated. In the search for magnetite receptors a large iron containing organelle (the cuticulosome) in the inner ear of pigeons was discovered.[54] [55] This organelle might represent part of an alternative magnetosensitive system. Taken together the receptor responsible for magnetosensitivity in homing pigeons remains uncertain.
Aside from the sensory receptor for magnetic reception in homing pigeons there has been work on neural regions that are possibly involved in the processing of magnetic information within the brain. Areas of the brain that have shown increases in activity in response to magnetic fields with a strength of 50 or 150 microtesla are the posterior vestibular nuclei, dorsal thalamus, hippocampus, and visual hyperpallium.[56]
In domestic hens
Domestic hens have iron mineral deposits in the dendrites in the upper beak and are capable of magnetoreception.[57][58]  Because hens use directional information from the magnetic field of the Earth to orient in relatively small areas, this raises the possibility that beak-trimming (removal of part of the beak, to reduce injurious pecking, frequently performed on egg-laying hens) impairs the ability of hens to orient in extensive systems, or to move in and out of buildings in free-range systems.[59]
In mammals

Work with mice, mole-rats and bats has shown that some mammals are capable of magnetoreception. When woodmice are removed from their home area and deprived of visual and olfactory cues, they orient themselves towards their homes until an inverted magnetic field is applied to their cage.[60] However, when the same mice are allowed access to visual cues, they are able to orient themselves towards home despite the presence of inverted magnetic fields. This indicates that when woodmice are displaced, they use magnetic fields to orient themselves if there are no other cues available. However, early studies of these subjects were criticized because of the difficulty of completely removing sensory cues, and in some because the tests were performed out of the natural environment. In others, the results of these experiments do not conclusively show a response to magnetic fields when deprived of other cues, because the magnetic field was artificially changed before the test rather than during it.[61]
Later research, accounting for those factors, has led to a conclusion that the Zambian mole-rat, a subterranean mammal, uses magnetic fields as a polarity compass to aid in the orientation of their nests.[61] In contrast to work with woodmice, Zambian mole-rats do not exhibit different orientation behavior when a visual cue such as the sun is present, a result that has been suggested is due to their subterranean lifestyle. Further investigation of mole-rat magnetoreception lead to the finding that exposure to magnetic fields leads to an increase in neural activity within the superior colliculus as measured by immediate early gene expression.[62] The activity level of neurons within  two levels of the superior colliculus, the outer sublayer of the intermediate gray layer and the deep gray layer, were elevated in a non-specific manner when exposed to various magnetic fields. However, within the inner sublayer of the intermediate gray layer (InGi) there were two or three clusters of responsive cells. The more time the mole rats were exposed to a magnetic field the greater the immediate early gene expression within the InGi. However, if Zambian mole-rats were placed in a field with a shielded magnetic field only a few scattered cells were active. Therefore, it has been proposed that in mammals, the superior colliculus is an important neural structure in the processing of magnetic information.
Bats may also use magnetic fields to orient themselves. While it is known that bats use echolocation to navigate over short distances, it is unclear how they navigate over longer distances.[63] When Eptesicus fuscus are taken from their home roosts and exposed to magnetic fields 90 degrees clockwise or counterclockwise of magnetic north, they are disoriented and set off for their homes in the wrong direction. Therefore, it seems that Eptesicus fuscus is capable of magnetoreception. However, the exact use of magnetic fields by Eptesicus fuscus is unclear as the magnetic field could be used either as a map, a compass, or a compass calibrator. Recent research with another bat species, Myotis myotis, supports the hypothesis that bats use magnetic fields as a compass calibrator and their primary compass is the sun.[64]
Red foxes (Vulpes vulpes) may use magnetoreception when predating small rodents. When foxes perform their high-jumps onto small prey like mice and voles, they tend to jump in a north-eastern compass direction. In addition, successful attacks are "tightly clustered" to the north.[65]  One study has found that when domestic dogs are off the leash and the Earth's magnetic field is calm, they prefer to urinate and defecate with their bodies aligned on a north-south axis.[66]
There is also evidence for magnetoreception in large mammals.  Resting and grazing cattle as well as roe deer (Capreolus capreolus) and red deer (Cervus elaphus) tend to align their body axes in the geomagnetic north-south direction.[67]  Because wind, sunshine, and slope could be excluded as common ubiquitous factors in this study, alignment toward the vector of the magnetic field provided the most likely explanation for the observed behaviour. However, because of the descriptive nature of this study, alternative explanations (e.g., the sun compass) could not be excluded.  In a follow-up study, researchers analyzed body orientations of ruminants in localities where the geomagnetic field is disturbed by high-voltage power lines to determine how local variation in magnetic fields may affect orientation behaviour.  This was done by using satellite and aerial images of herds of cattle and field observations of grazing roe deer.  Body orientation of both species was random on pastures under or near power lines.  Moreover, cattle exposed to various magnetic fields directly beneath or in the vicinity of power lines trending in various magnetic directions exhibited distinct patterns of alignment.  The disturbing effect of the power lines on body alignment diminished with the distance from the conductors.[68] In 2011 a group of Czech researchers, however, reported their failed attempt to replicate the finding using different Google Earth images.[69]
Humans "are not believed to have a magnetic sense", but humans do have a cryptochrome (a flavoprotein, CRY2) in the retina which has a light-dependent magnetosensitivity. CRY2 "has the molecular capability to function as a light-sensitive magnetosensor", so the area was thought (2011) to be ripe for further study.[2]
Issues
Despite more than 50 years of research, a sensory receptor in animals has yet to be identified for magnetoreception.[70] While research is ongoing, it is possible that the entire receptor system could fit in a one-milimeter cube and have a magnetic content of less than one ppm. As such, even discerning the parts of the brain where the information is processed presents a challenge.[71]
The most promising leads — cryptochromes, iron-based systems, electromagnetic induction — each have their own pros and cons. Cryptochromes have been observed in various organisms including birds and humans, but does not answer the question of night-time navigation. Iron-based systems have also been observed in birds, and if proven, could form a magnetoreceptive basis for many species including turtles. Electromagnetic induction has not been observed nor tested in non-aquatic animals. Additionally, it remains likely that two or more complementary mechanisms play a role in magnetic field detection in animals. Of course, this potential dual mechanism theory raises the question, to what degree is each method responsible for the stimulus, and how do they produce a signal in response to the low magnetic field of the Earth?[72]
Then there is the distinction of magnetic usage. Some species may only be able to sense a magnetic compass to find north and south, while others may only be able to discern between the equator and the pole. Although the ability to sense direction is important in migratory navigation, many animals also have the ability to sense small fluctuations in earth’s magnetic field to compute coordinate maps with a resolution of a few kilometers or better.[73] For a magnetic map, the receptor system would have to be able to discern tiny differences in the surrounding magnetic field to develop a sufficiently detailed magnetic map. This is not out of the question, as many animals have the ability to sense small fluctuations in the earth's magnetic field. This is not out of the question biologically, but physically has yet to be explained. For example, birds such as the homing pigeon are believed to use the magnetite in their beaks to detect magnetic signposts and thus, the magnetic sense they gain from this pathway is a possible map.[72] Yet, it has also been suggested that homing pigeons and other birds use the visually mediated cryptochrome receptor as a compass.[72]

See also
Magnetobiology
Quantum biology §Magnetoreception
Salmon run



, Theoretical and Biophysical Computations Group, University of Illinois at Urbana–Champaign