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. In navigation, magnetoreception deals with the detection of the Earth's magnetic field.

The homing pigeon can return to its home using its ability to sense the Earth's magnetic field and other cues to orient itself

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

In 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. 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 are two main hypotheses being currently discussed: one proposing a chemical compass based on a radical pair mechanism, the other postulating processes involving magnetite particles.[4] According to the first model, magnetoreception is possible via the radical pair mechanism,[5] which is well-established in spin chemistry[6][7][8] 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.[5] 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.[9] The Earth's magnetic field is only 0.5 gauss and radical pair mechanism is the only plausible way that weak magnetic fields can affect chemical changes.[10] Cryptochromes are therefore thought to be essential for the light-dependent ability of the fruit fly Drosophila melanogaster to sense magnetic fields.[11]

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,[12] but also in other taxa.[13]

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.[14][15] 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.[16]

Maghemite has been observed in platelet-like structures concentrated along the sensory 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.[17] 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.[15]

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

.

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.[18][19] 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.[20]

Endosymbiotic magnetotactic bacteria

A more recent proposed explanation of magnetoreception in animals is through endosymbiosis with magnetotactic bacteria. This appears at least plausible, as the DNA of these bacteria is widespread in animals.[21]

In invertebrates

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.

Fruit fly Drosophila melanogaster needs cryptochrome to respond to magnetic fields.

The fruit fly 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.[11] 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 420 nm 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 350 nm – 400 nm and plateaus from 430-450 nm.[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 insects including 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]

In fish, amphibians and reptiles

Magnetoreception has been reported in the European eel,[35] while 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 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.[39]

Magnetoreception plays a part in guiding Loggerhead hatchlings to the sea

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.[41] 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.[42]

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.[43]

In homing pigeons

Homing pigeons can use magnetic fields as part of their complex navigation system.[44] William Keeton showed that time-shifted homing pigeons (acclimatised in the laboratory to a different time-zone) are unable to orient themselves correctly on a clear, sunny day; this 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.[45] 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.[46] More recent behavioral tests have shown that pigeons are able to detect magnetic anomalies of 186 microtesla (1.86 Gauss).[47]

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.[48] Subsequent studies, however, revealed that these cells were macrophages, not magnetosensitive neurons.[49][50] Second, pigeon magnetic field detection is impaired by sectioning the trigeminal nerve and by application of lidocaine, an anesthetic, to the olfactory mucosa.[51] However, lidocaine treatment might lead to unspecific effects and not represent a direct interference with potential magnetoreceptors.[50] Therefore, an involvement 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.[52][53] 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.[54]

In domestic hens

Domestic hens have iron mineral deposits in the sensory dendrites in the upper beak and are capable of magnetoreception.[55][56] 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.[57]

In mammals
Several mammals, including the big brown bat (Eptesicus fuscus) can use magnetic fields for orientation.

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.[58] 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.[59] Recent experiments, however, confirmed that woodmice have a magnetic sense which is likely based on a radical-pair mechanism.[60]

The Zambian mole-rat, a subterranean mammal, uses magnetic fields as a polarity compass to aid in the orientation of their nests.[59] In contrast to woodmice, Zambian mole-rats do not rely on radical-pair based magnetoreception, 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.[61] 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 cells that respond in a more specific manner. 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.[62] 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.[63]

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.[64] One study has found that when domestic dogs (Canis lupus familiaris) 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.[65]

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.[66] 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.[67] In 2011 a group of Czech researchers, however, reported their failed attempt to replicate the finding using different Google Earth images.[68]

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] A 2019 study found that magnetic fields do affect human alpha brain waves, but it is not known whether this results in any change in behavior. [69]

Issues

Despite more than 50 years of research, a sensory receptor in animals has yet to be identified for magnetoreception.[70] It is possible that the entire receptor system could fit in a one-millimeter 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?[17]

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.[72] 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.[17] Yet, it has also been suggested that homing pigeons and other birds use the visually mediated cryptochrome receptor as a compass.[17]

See also

References
  1. Wiltschko, F. R. & Wiltschko, W. (2012). "Chapter 8 - Magnetoreception". In Carlos López-Larrea (ed.). Sensing in Nature. Advances in Experimental Medicine and Biology. 739. Springer. doi:10.1007/978-1-4614-1704-0. ISBN 978-1-4614-1703-3. S2CID 41131723.
  2. Foley, Lauren E.; Gegear, Robert J.; Reppert, Steven M. (2011). "Human cryptochrome exhibits light-dependent magnetosensitivity". Nature Communications. 2: 356. Bibcode:2011NatCo...2..356F. doi:10.1038/ncomms1364. PMC 3128388. PMID 21694704.
  3. Blakemore, R. (1975). "Magnetotactic Bacteria". Science. 190 (4212): 377–379. Bibcode:1975Sci...190..377B. doi:10.1126/science.170679. PMID 170679. S2CID 5139699.
  4. Wiltschko, Wolfgang; Wiltschko, Roswitha (August 2008). "Magnetic orientation and magnetoreception in birds and other animals". Journal of Comparative Physiology A. 191 (8): 675–693. doi:10.1007/s00359-005-0627-7. PMID 15886990. S2CID 206960525.
  5. Hore, P.J.; Mouritsen, Henrik (5 July 2016). "The Radical-Pair Mechanism of Magnetoreception". Annual Review of Biophysics. 45 (1): 299–344. doi:10.1146/annurev-biophys-032116-094545. PMID 27216936.
  6. T., Rodgers, Christopher (1 January 2009). "Magnetic field effects in chemical systems". Pure and Applied Chemistry. 81 (1): 19–43. doi:10.1351/PAC-CON-08-10-18. ISSN 1365-3075. S2CID 96850994.
  7. Steiner, Ulrich E.; Ulrich, Thomas (1 January 1989). "Magnetic field effects in chemical kinetics and related phenomena". Chemical Reviews. 89 (1): 51–147. doi:10.1021/cr00091a003. ISSN 0009-2665.
  8. Woodward, J. R. (1 September 2002). "Radical pairs in solution". Progress in Reaction Kinetics and Mechanism. 27 (3): 165–207. doi:10.3184/007967402103165388. S2CID 197049448.
  9. Wiltschko, Roswitha; Ahmad, Margaret; Nießner, Christine; Gehring, Dennis; Wiltschko, Wolfgang (1 May 2016). "Light-dependent magnetoreception in birds: The crucial step occurs in the dark". Journal of the Royal Society, Interface. 13 (118): 20151010. doi:10.1098/rsif.2015.1010. ISSN 1742-5662. PMC 4892254. PMID 27146685.
  10. Rodgers, C. T.; Hore, P. J. (2009). "Chemical magnetoreception in birds: The radical pair mechanism". Proceedings of the National Academy of Sciences of the United States of America. 106 (2): 353–360. Bibcode:2009PNAS..106..353R. doi:10.1073/pnas.0711968106. PMC 2626707. PMID 19129499.
  11. Gegear, Robert J.; Casselman, Amy; Waddell, Scott; Reppert, Steven M. (August 2008). "Cryptochrome mediates light-dependent magnetosensitivity in Drosophila". Nature. 454 (7207): 1014–1018. Bibcode:2008Natur.454.1014G. doi:10.1038/nature07183. PMC 2559964. PMID 18641630.
  12. Fleissner, Gerta; Holtkamp-Rötzler, Elke; Hanzlik, Marianne; Winklhofer, Michael; Fleissner, Günther; Petersen, Nikolai; Wiltschko, Wolfgang (26 February 2003). "Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons". Journal of Comparative Neurology. 458 (4): 350–360. doi:10.1002/cne.10579. ISSN 0021-9967. PMID 12619070. S2CID 36992055.
  13. Fleissner, Guenther; Wellenreuther, Gerd; Heyers, Dominik; Mouritsen, Henrik; Thalau, Peter; Kuehbacher, Markus; Schuchardt, Kirsten; Fleissner, Gerta; Falkenberg, Gerald (16 February 2010). "Avian Magnetoreception: Elaborate Iron Mineral Containing Dendrites in the Upper Beak Seem to Be a Common Feature of Birds". PLOS ONE. 5 (2): e9231. Bibcode:2010PLoSO...5.9231F. doi:10.1371/journal.pone.0009231. ISSN 1932-6203. PMC 2821931. PMID 20169083.
  14. Hore, P. J.; Mouritsen, Henrik (5 July 2016). "The Radical-Pair Mechanism of Magnetoreception". Annual Review of Biophysics. 45 (1): 299–344. doi:10.1146/annurev-biophys-032116-094545. ISSN 1936-122X. PMID 27216936.
  15. Solov’yov, Ilia A.; Greiner, Walter (September 2007). "Theoretical Analysis of an Iron Mineral-Based Magnetoreceptor Model in Birds". Biophysical Journal. 93 (5): 1493–1509. Bibcode:2007BpJ....93.1493S. doi:10.1529/biophysj.107.105098. ISSN 0006-3495. PMC 1948037. PMID 17496012.
  16. Keays, David Anthony; Shaw, Jeremy; Lythgoe, Mark; Saunders, Martin; Cadiou, Herve; Pichler, Paul; Breuss, Martin; Sugar, Cristina; Edelman, Nathaniel (April 2012). "Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons". Nature. 484 (7394): 367–370. Bibcode:2012Natur.484..367T. doi:10.1038/nature11046. ISSN 1476-4687. PMID 22495303. S2CID 205228624.
  17. Rodgers, C. T.; Hore, P. J. (2009). "Chemical magnetoreception in birds: The radical pair mechanism". Proceedings of the National Academy of Sciences of the United States of America. 106 (2): 353–360. Bibcode:2009PNAS..106..353R. doi:10.1073/pnas.0711968106. PMC 2626707. PMID 19129499.
  18. Blonder, Barbara I.; Alevizon, William S. (1988). "Prey Discrimination and Electroreception in the Stingray Dasyatis sabina". Copeia. 1988 (1): 33–36. doi:10.2307/1445919. JSTOR 1445919.
  19. Kalmijn, A. J. (1 October 1971). "The Electric Sense of Sharks and Rays". Journal of Experimental Biology. 55 (2): 371–383. ISSN 0022-0949. PMID 5114029.
  20. Nordmann, Gregory C.; Hochstoeger, Tobias; Keays, David A. (23 October 2017). "Magnetoreception—A sense without a receptor". PLOS Biology. 15 (10): e2003234. doi:10.1371/journal.pbio.2003234. ISSN 1545-7885. PMC 5695626. PMID 29059181.
  21. Natan, Eviatar; Fitak, Robert Rodgers; Werber, Yuval; Vortman, Yoni (28 September 2020). "Symbiotic magnetic sensing: raising evidence and beyond". Philosophical Transactions of the Royal Society B: Biological Sciences. 375 (1808): 20190595. doi:10.1098/rstb.2019.0595. PMC 7435164. PMID 32772668.
  22. Vidal-Gadea, A.G.; Ward, K.; Beron, C.; Ghorashian, N.; Gokce, S.; Russell, J.; Truong, N.; Parikh, A.; Gadea, G.; Ben-Yakar, A.; Pierce-Shimomura, J. (2015). "Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans". eLife. 4. doi:10.7554/eLife.07493. PMC 4525075. PMID 26083711.
  23. Landler, Lukas; Nimpf, Simon; Hochstoeger, Tobias; Nordmann, Gregory C; Papadaki-Anastasopoulou, Artemis; Keays, David A (13 April 2018). "Comment on "Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans"". eLife. 7. doi:10.7554/elife.30187. ISSN 2050-084X. PMC 5898909. PMID 29651983.
  24. Landler, Lukas; Nordmann, Gregory; Nimpf, Simon; Hochstoeger, Tobias; Kagerbauer, Daniel; Keays, David (18 June 2018). "Revised testing procedures do not elicit magnetoreceptive behavior in C. elegans". bioRxiv 10.1101/349944.
  25. Lohmann, K. J.; Willows, A. O. D. (1987). "Lunar-Modulated Geomagnetic Orientation by a Marine Mollusk". Science. 235 (4786): 331–334. Bibcode:1987Sci...235..331L. doi:10.1126/science.3798115. PMID 3798115.
  26. Lohmann, K. J.; Willows; Pinter, R. B. (1991). "An identifiable molluscan neuron responds to changes in earth-strength magnetic fields". The Journal of Experimental Biology. 161: 1–24. PMID 1757771.
  27. Wang, J. H. (2004). "Identifiable neurons inhibited by Earth-strength magnetic stimuli in the mollusc Tritonia diomedea". Journal of Experimental Biology. 207 (6): 1043–1049. doi:10.1242/jeb.00864. PMID 14766962. S2CID 13439801.
  28. VanVickle-Chavez, S.J.; Van Gelder, R. N. (2007). "Action Spectrum of Drosophila Cryptochrome *". Journal of Biological Chemistry. 282 (14): 10561–10566. doi:10.1074/jbc.M609314200. PMID 17284451. S2CID 19684507.
  29. Gegear, R. J.; Foley, L. E.; Casselman, A.; Reppert, S. M. (2010). "Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism". Nature. 463 (7282): 804–7. Bibcode:2010Natur.463..804G. doi:10.1038/nature08719. PMC 2820607. PMID 20098414.
  30. Quinn, Thomas P. (1980). "Evidence for celestial and magnetic compass orientation in lake migrating sockeye salmon fry". Journal of Comparative Physiology A. 137 (3): 243–248. doi:10.1007/bf00657119. ISSN 0340-7594. S2CID 44036559.
  31. Taylor, P. B. (May 1986). "Experimental evidence for geomagnetic orientation in juvenile salmon, Oncorhynchus tschawytscha Walbaum". Journal of Fish Biology. 28 (5): 607–623. doi:10.1111/j.1095-8649.1986.tb05196.x. ISSN 0022-1112.
  32. Pereira-Bomfim, M.D.G.C.; Antonialli-Junior, W.F.; Acosta-Avalos, D. (2015). "Effect of magnetic field on the foraging rhythm and behavior of the swarm-founding paper wasp Polybia paulista Ihering (hymenoptera: vespidae)". Sociobiology. 62 (1): 99–104. doi:10.13102/sociobiology.v62i1.99-104.
  33. Wajnberg, E.; Acosta-Avalos, D.; Alves, O.C.; de Oliveira, J.F.; Srygley, R.B.; Esquivel, D.M. (2010). "Magnetoreception in eusocial insects: An update". Journal of the Royal Society Interface. 7 (Suppl 2): S207–S225. doi:10.1098/rsif.2009.0526.focus. PMC 2843992. PMID 20106876.
  34. Nunes, T.M.; Turatti, I.C.C.; Mateus, S.; Nascimento, F.S.; Lopes, N.P.; Zucchi, R. (2009). "Cuticular Hydrocarbons in the Stingless Bee Schwarziana quadripunctata (Hymenoptera, Apidae, Meliponini): Differences between Colonies, Castes and Age". Genetics and Molecular Research. 8 (2): 589–595. doi:10.4238/vol8-2kerr012. PMID 19551647.
  35. Eels May Use 'Magnetic Maps' As They Slither Across The Ocean
  36. Phillips, John B. (1977). "Use of the earth's magnetic field by orienting cave salamanders (Eurycea lucifuga)". Journal of Comparative Physiology. 121 (2): 273–288. doi:10.1007/bf00609616. ISSN 0340-7594. S2CID 44654348.
  37. Phillips, John B. (1986). "Magnetic compass orientation in the Eastern red-spotted newt (Notophthalmus viridescens)". Journal of Comparative Physiology A. 158 (1): 103–109. doi:10.1007/bf00614524. ISSN 0340-7594. PMID 3723427. S2CID 25252103.
  38. Phillips, J. (15 August 1986). "Two magnetoreception pathways in a migratory salamander". Science. 233 (4765): 765–767. Bibcode:1986Sci...233..765P. doi:10.1126/science.3738508. ISSN 0036-8075. PMID 3738508. S2CID 28292152.
  39. Sinsch, Ulrich (1987). "Orientation behaviour of toads (Bufo bufo) displaced from the breeding site". Journal of Comparative Physiology A. 161 (5): 715–727. doi:10.1007/bf00605013. ISSN 0340-7594. PMID 3119823. S2CID 26102029.
  40. Sinsch, Ulrich (January 1992). "Sex-biassed site fidelity and orientation behaviour in reproductive natterjack toads (Bufo calamita)". Ethology Ecology & Evolution. 4 (1): 15–32. doi:10.1080/08927014.1992.9525347. ISSN 0394-9370.
  41. Mathis, Alicia; Moore, Frank R. (26 April 2010). "Geomagnetism and the Homeward Orientation of the Box Turtle, Terrapene Carolina". Ethology. 78 (4): 265–274. doi:10.1111/j.1439-0310.1988.tb00238.x. ISSN 0179-1613.
  42. G., Stehli, F. (1996). Magnetite Biomineralization and Magnetoreception in Organisms: A new biomagnetism. US: Springer. ISBN 9781461303138. OCLC 958527742.
  43. Merrill, Maria W.; Salmon, Michael (30 September 2010). "Magnetic orientation by hatchling loggerhead sea turtles (Caretta caretta) from the Gulf of Mexico". Marine Biology. 158 (1): 101–112. doi:10.1007/s00227-010-1545-y. ISSN 0025-3162. S2CID 84391053.
  44. Walcott, C. (1996). "Pigeon homing: observations, experiments and confusions". The Journal of Experimental Biology. 199 (Pt 1): 21–7. PMID 9317262.
  45. Keeton, W. T. (1971). "Magnets interfere with pigeon homing". Proceedings of the National Academy of Sciences of the United States of America. 68 (1): 102–6. Bibcode:1971PNAS...68..102K. doi:10.1073/pnas.68.1.102. PMC 391171. PMID 5276278.
  46. Gould, J. L. (1984). "Magnetic field sensitivity in animals". Annual Review of Physiology. 46: 585–98. doi:10.1146/annurev.ph.46.030184.003101. PMID 6370118.
  47. Mora, C. V.; Davison, M.; Wild, J. M.; Walker, M. M. (2004). "Magnetoreception and its trigeminal mediation in the homing pigeon". Nature. 432 (7016): 508–511. Bibcode:2004Natur.432..508M. doi:10.1038/nature03077. PMID 15565156. S2CID 2485429.
  48. Fleissner, Gerta; Holtkamp-Rötzler, Elke; Hanzlik, Marianne; Winklhofer, Michael; Fleissner, Günther; Petersen, Nikolai; Wiltschko, Wolfgang (26 February 2003). "Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons". Journal of Comparative Neurology. 458 (4): 350–360. doi:10.1002/cne.10579. ISSN 0021-9967. PMID 12619070. S2CID 36992055.
  49. Treiber, Christoph Daniel; Salzer, Marion Claudia; Riegler, Johannes; Edelman, Nathaniel; Sugar, Cristina; Breuss, Martin; Pichler, Paul; Cadiou, Herve; Saunders, Martin (11 April 2012). "Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons". Nature. 484 (7394): 367–70. Bibcode:2012Natur.484..367T. doi:10.1038/nature11046. ISSN 0028-0836. PMID 22495303. S2CID 205228624.
  50. Engels, Svenja; Treiber, Christoph Daniel; Salzer, Marion Claudia; Michalik, Andreas; Ushakova, Lyubo v; Keays, David Anthony; Mouritsen, Henrik; Heyers, Dominik (1 August 2018). "Lidocaine is a nocebo treatment for trigeminally mediated magnetic orientation in birds". Journal of the Royal Society Interface. 15 (145): 20180124. doi:10.1098/rsif.2018.0124. ISSN 1742-5689. PMC 6127160. PMID 30089685.
  51. Wiltschko, Roswitha; Schiffner, Ingo; Fuhrmann, Patrick; Wiltschko, Wolfgang (September 2010). "The Role of the Magnetite-Based Receptors in the Beak in Pigeon Homing". Current Biology. 20 (17): 1534–1538. Bibcode:1996CBio....6.1213A. doi:10.1016/j.cub.2010.06.073. ISSN 0960-9822. PMID 20691593. S2CID 15896143.
  52. Lauwers, Mattias; Pichler, Paul; Edelman, Nathaniel Bernard; Resch, Guenter Paul; Ushakova, Lyubov; Salzer, Marion Claudia; Heyers, Dominik; Saunders, Martin; Shaw, Jeremy (May 2013). "An Iron-Rich Organelle in the Cuticular Plate of Avian Hair Cells". Current Biology. 23 (10): 924–929. Bibcode:1996CBio....6.1213A. doi:10.1016/j.cub.2013.04.025. ISSN 0960-9822. PMID 23623555. S2CID 9052155.
  53. Nimpf, Simon; Malkemper, Erich Pascal; Lauwers, Mattias; Ushakova, Lyubov; Nordmann, Gregory; Wenninger-Weinzierl, Andrea; Burkard, Thomas R; Jacob, Sonja; Heuser, Thomas (15 November 2017). "Subcellular analysis of pigeon hair cells implicates vesicular trafficking in cuticulosome formation and maintenance". eLife. 6. doi:10.7554/elife.29959. ISSN 2050-084X. PMC 5699870. PMID 29140244.
  54. Wu, L.-Q.; Dickman, J. D. (2011). "Magnetoreception in an avian brain in part mediated by inner ear lagena". Current Biology. 21 (5): 418–23. doi:10.1016/j.cub.2011.01.058. PMC 3062271. PMID 21353559.
  55. Falkenberg, G.; Fleissner, G.; Schuchardt, K.; Kuehbacher, M.; Thalau, P.; Mouritsen, H.; Heyers, D.; Wellenreuther, G.; Fleissner, G. (2010). "Avian magnetoreception: Elaborate iron mineral containing dendrites in the upper beak seem to be a common feature of birds". PLOS ONE. 5 (2): e9231. Bibcode:2010PLoSO...5.9231F. doi:10.1371/journal.pone.0009231. PMC 2821931. PMID 20169083.
  56. Wiltschko, W., Freire, R., Munro, U., Ritz, T., Rogers, L.J., Thalau, P., and Wiltschko. R., (2007). The magnetic compass of domestic chicken, Gallus gallus. Journal Experimental Biology, 210:2300–2310
  57. Freire, R.; Eastwood, M.A.; Joyce, M. (2011). "Minor beak trimming in chickens leads to loss of mechanoreception and magnetoreception". Journal of Animal Science. 89 (4): 1201–1206. doi:10.2527/jas.2010-3129. PMID 21148779.
  58. Mather, J.G.; Baker, R. R. (1981). "Magnetic sense of direction in woodmice for route-based navigation". Nature. 291 (5811): 152–155. Bibcode:1981Natur.291..152M. doi:10.1038/291152a0. S2CID 4262309.
  59. Marhold, S.; Wiltschko, W.; Burda, H. (1997). "A magnetic polarity compass for direction finding in a subterranean mammal". Naturwissenschaften. 84 (9): 421–423. Bibcode:1997NW.....84..421M. doi:10.1007/s001140050422. S2CID 44399837.
  60. Malkemper, E. Pascal; Eder, Stephan H. K.; Begall, Sabine; Phillips, John B.; Winklhofer, Michael; Hart, Vlastimil; Burda, Hynek (29 April 2015). "Magnetoreception in the wood mouse ( Apodemus sylvaticus ): influence of weak frequency-modulated radio frequency fields". Scientific Reports. 5 (1): 9917. Bibcode:2015NatSR...4E9917M. doi:10.1038/srep09917. ISSN 2045-2322. PMC 4413948. PMID 25923312.
  61. Nemec, P.; Altmann, J.; Marhold, S.; Burda, H.; Oelschlager, H. H. (2001). "Neuroanatomy of magnetoreception: The superior colliculus involved in magnetic orientation in a mammal". Science. 294 (5541): 366–8. Bibcode:2001Sci...294..366N. doi:10.1126/science.1063351. PMID 11598299. S2CID 41104477.
  62. Holland, R. A.; Thorup, K.; Vonhof, M. J.; Cochran, W. W.; Wikelski, M. (2006). "Bat orientation using Earth's magnetic field". Nature. 444 (7120): 702. Bibcode:2006Natur.444..702H. doi:10.1038/444702a. PMID 17151656. S2CID 4379579.
  63. Wiltschko, R.; Wiltschko, W. (2006). "Magnetoreception". BioEssays. 28 (2): 157–68. doi:10.1002/bies.20363. PMID 16435299. S2CID 221464152.
  64. "Fox 'rangefinder' sense expands the magnetic menagerie". blogs.nature.com. Nature Publishing Group / Macmillan. Retrieved 6 June 2014.
  65. Hart, Vlastimil; Nováková, Petra; Malkemper, Erich Pascal; Begall, Sabine; Hanzal, Vladimír; Ježek, Miloš; Kušta, Tomáš; Němcová, Veronika; Adámková, Jana; Benediktová, Kateřina; Červený, Jaroslav; Burda, Hynek (2013). "Dogs are sensitive to small variations of the Earth's magnetic field". Frontiers in Zoology. 10 (1): 80. doi:10.1186/1742-9994-10-80. PMC 3882779. PMID 24370002.
  66. Begall, S.; Cerveny, J.; Neef, J.; Vojtech, O.; Burda, H. (2008). "Magnetic alignment in grazing and resting cattle and deer". Proc. Natl. Acad. Sci. U.S.A. 105 (36): 13451–13455. Bibcode:2008PNAS..10513451B. doi:10.1073/pnas.0803650105. PMC 2533210. PMID 18725629.
  67. Burda, H.; Begalla, S.; Červený, J.; Neefa, J.; Němecd, P. (2009). "Extremely low-frequency electromagnetic fields disrupt magnetic alignment of ruminants". Proc. Natl. Acad. Sci. USA. 106 (14): 5708–5713. Bibcode:2009PNAS..106.5708B. doi:10.1073/pnas.0811194106. PMC 2667019. PMID 19299504.
  68. Hert, J; Jelinek, L; Pekarek, L; Pavlicek, A (2011). "No alignment of cattle along geomagnetic field lines found". Journal of Comparative Physiology. 197 (6): 677–682. arXiv:1101.5263. Bibcode:2011arXiv1101.5263H. doi:10.1007/s00359-011-0628-7. PMID 21318402. S2CID 15520857.
  69. Wang, Connie (18 March 2019). "Transduction of the Geomagnetic Field as Evidenced from alpha-Band Activity in the Human Brain". eNeuro. 6 (2): ENEURO.0483–18.2019. doi:10.1523/ENEURO.0483-18.2019. PMC 6494972. PMID 31028046. S2CID 84835867. Retrieved 5 November 2020.
  70. Gould, J. L. (1984). "Magnetic field sensitivity in animals". Annual Review of Physiology. 46: 585–98. doi:10.1146/annurev.ph.46.030184.003101. PMID 6370118.
  71. Kirschvink, J.L. (1997). "Magnetoreception: Homing in on vertebrates". Nature. 390 (6658): 339–340. Bibcode:1997Natur.390..339K. doi:10.1038/36986. S2CID 5189690.
  72. Gould, J. L. (2008). "Animal navigation: The evolution of magnetic orientation". Current Biology. 18 (11): R482–R48. doi:10.1016/j.cub.2008.03.052. PMID 18522823. S2CID 10961495.
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