Magnetic orientation and magnetoreception in birds and other animals
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- Wiltschko, W. & Wiltschko, R. J Comp Physiol A (2005) 191: 675. doi:10.1007/s00359-005-0627-7
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Animals use the geomagnetic field in many ways: the magnetic vector provides a compass; magnetic intensity and/or inclination play a role as a component of the navigational ‘map’, and magnetic conditions of certain regions act as ‘sign posts’ or triggers, eliciting specific responses. A magnetic compass is widespread among animals, magnetic navigation is indicated e.g. in birds, marine turtles and spiny lobsters and the use of magnetic ‘sign posts’ has been described for birds and marine turtles. For magnetoreception, two hypotheses are currently discussed, one proposing a chemical compass based on a radical pair mechanism, the other postulating processes involving magnetite particles. The available evidence suggests that birds use both mechanisms, with the radical pair mechanism in the right eye providing directional information and a magnetite-based mechanism in the upper beak providing information on position as component of the ‘map’. Behavioral data from other animals indicate a light-dependent compass probably based on a radical pair mechanism in amphibians and a possibly magnetite-based mechanism in mammals. Histological and electrophysiological data suggest a magnetite-based mechanism in the nasal cavities of salmonid fish. Little is known about the parts of the brain where the respective information is processed.
The geomagnetic field
Many animals are able to perceive the magnetic field of the earth; among them are mollusks, arthropods and members of all major groups of vertebrates. This seems alien to us, as man cannot consciously sense the geomagnetic field (but see Baker 1989). To fully understand this phenomenon, we must first consider the type of information the geomagnetic field can provide and—even more important—the type of information animals do actually use.
The geomagnetic field thus represents a reliable, omnipresent source of navigational information. This information can be of two kinds: the magnetic vector provides directional information that animals could use as a compass, whereas total intensity and/or inclination may provide information that might be used as a component of the navigational ‘map’ indicating position.
Animals have been shown to use both types of information for various tasks. However, our knowledge on magnetic orientation differs greatly between the various animals. Birds are by far the best studied group, followed by marine turtles, while little is known about other vertebrates and arthropods. Here, we summarize the findings that are most important in demonstrating how widespread the use of magnetic information is and what types of information the animals utilize.
Magnetic compass orientation
A magnetic compass means that directions can be determined with the help of the magnetic field. In orientation experiments, the observation that an animal responds to shift in magnetic North with a corresponding change in its heading is diagnostic of magnetic compass use.
Demonstrating magnetic compass orientation
A magnetic compass appears to be rather widespread among animals. It was first demonstrated in migratory birds, taking advantage of a spontaneous behavior: during migration season, the urge of migrants to move into migratory direction is so strong that even captive birds head into the respective direction in their cages. When tested in the local geomagnetic field, European robins, Erithacus rubecula, but also other species of migrants, showed a strong preference of their seasonally appropriate migratory direction. Tested in an experimental field of equal intensity, but with magnetic North turned by a certain angle with the help of Helmholtz coils, the same birds altered their headings accordingly and preferred the direction that now corresponded to the same magnetic course (Fig. 2, left, center). This clearly shows that robins used the geomagnetic field to orient their movements (see Wiltschko and Wiltschko 1995 for details).
Animals demonstrated to use a magnetic compass (numbers in parentheses give the number of species where the respective type of compass is indicated; ??? means that the type of compass has not yet been analyzed)
No. of orders
No. of families
No. of species
Type of compass?
Polarity compass (1)
Polarity compass? (1)
Polarity compass? (1)
Inclination compass (1)
Inclination compass (2)
Inclination compass (8)
Polarity compass (1)
Functional mode of magnetic compass mechanisms
The functional mode of the magnetic compass was first analyzed in birds, again with the help of migratory orientation. Two unexpected properties became evident.
Non-compass use of the magnetic field
Because of their nature as gradients running from north to south, magnetic intensity and inclination can give information on position. Evidence for this use of magnetic information is much rarer than that supporting compass use, and the number of species involved is much smaller.
Magnetic intensity has been discussed as a component of the navigational ‘map’ of pigeons ever since the late nineteenth century (Viguier 1882). It could be used in the following way: in the northern hemisphere, birds know by experience that magnetic intensity increases towards north; when finding themselves at a location with intensity higher than at home, they would conclude that they are north of home and hence must head south to return. The intensity difference to be detected for magnetic navigation within the home range would be in the order of magnitude of 20 to 100 nT, the differences in inclination in fractions of a degree, depending on the regional gradients and the distances involved.
First indications that animals use magnetic parameters in their navigational ‘map’ came from correlations of the vanishing bearings of homing pigeons, Columba livia f. domestica, with temporal changes of the magnetic field (e.g. Keeton et al. 1974). Pigeons released in a magnetic anomaly showed an increase in scatter up to disorientation that was strongly correlated with steepness of the local intensity gradient (Walcott 1978). The effects of various magnetic treatments on pigeons’ initial orientation that cannot be attributed to interfering with the magnetic compass also suggested an involvement of magnetic factors in the navigational process (for summary, see Wiltschko and Wiltschko 1995). Migratory Australian Silvereyes, Zosterops lateralis, also responded to slight changes in magnetic intensity and inclination (Fisher et al. 2003).
Magnetic conditions as ‘sign posts’ or triggers
Implications for magnetoreception
The behavioral evidence summarized above clearly shows that magnetoreception is not a uniform phenomenon: animals use different parameters of the geomagnetic field in different tasks. The nature of these parameters makes it rather unlikely that they are detected by the same mechanism. The magnetic compass does not respond to the small differences in intensity whose detection is crucial for using magnetic intensity as component of the navigational ‘map’; these small changes are well within the functional window of the compass mechanism and are thus filtered off. Likewise, a mechanism designed to record tiny changes in intensity can, at the same time, hardly measure the direction of the magnetic field with great precision. Hence we must expect animals to have specialized receptors for mediating magnetic intensity and others for mediating information on magnetic direction, just as we use different technical devices – a compass and a magnetometer – to measure the direction and the intensity of the magnetic field. Additionally, the two types of magnetic compass – inclination compass and polarity compass – imply that here, too, different mechanisms may be involved.
For a complete understanding of a ‘magnetic sense’, one needs to know (1) details on the primary processes mediating magnetic input, (2) the location of the sensory organ, its structure and its connections to the central nervous system and (3) what parts of the brain are involved in processing magnetic information. Unfortunately, our knowledge on the physiological and neurobiological processes associated with magnetoreception is still rather limited. The various animal groups are not equally represented: birds are by far the best studied group; fish are the only other group where some neuroanatomical and electrophysiological evidence is available.
A number of models for magnetoreception based on fundamentally different principles have been proposed, the three most prominent ones being (1) induction, (2) interactions of chemical processes with the ambient magnetic field and (3) processes involving permanently magnetic material.
Induction would be restricted to marine animals because it requires sea water as a surrounding medium with high conductivity. When skates and rays swim into different directions, they cross the field lines of the geomagnetic field at different angles, thus inducing different voltages at their electric organs (Murray 1962). The ampullary organs of skates and rays are known to be sensitive enough to detect the differences in voltage induced when the fish are heading in different directions (e.g. Kalmijn 1978), but evidence that this information is indeed used to derive compass orientation is still lacking.
The other two models – the ‘radical pair’-model and the magnetite-hypothesis – are more general and would also serve terrestrial animals and those living in fresh water.
Magnetoreception based on ‘radical pair’-mechanisms, and associated findings
The radical pair model, first proposed by Schulten and Windemuth (1986) and later detailed by Ritz et al. (2000), postulates a ‘chemical compass’ based on direction-specific interactions of radical pairs with the ambient magnetic field. It is supported by experimental evidence in birds and amphibians.
To obtain magnetic compass information by a radical pair mechanism, animals must take advantage of the fact that triplet products are chemically different from singlet products and compare the triplet yields in different directions. This requires an orderly array of photopigments oriented in the various spatial directions. These conditions could be met by the more or less spherical arrangement of receptors in the eyes – radical pair processes would generate characteristic patterns of activation across the retina (Ritz et al. 2000). These patterns whose specific manifestations depend on magnetic intensity, would be centrally symmetric around the axis of the field lines, that is, axial rather than polar, and would enable animals to detect the direction of the ambient field. At the same time, the initial photon absorption would make magnetoreception a light-dependent process.
Evidence supporting the radical pair model
Because of the axial pattern of activation, a radical pair mechanism would provide an inclination compass. Hence the radical pair model can only apply to the magnetic compass of birds, amphibians and marine turtles (see Table 1). In birds, this model also provides an explanation for the narrow functional window of the magnetic compass that can be altered by exposing them to magnetic intensities outside the normal functional range (see Fig. 5): when tested under intensities that differ markedly from that of the local geomagnetic field, the birds would be faced with a novel activation pattern (Ritz et al. 2000). This may confuse them at first, yet the pattern retains its central symmetry around the axis of the field lines. Given sufficient time, the birds may become familiar with the novel pattern and learn to interpret it, thus regaining their ability to orient.
The radical pair model predicts that magnetoreception is light-dependent. Light is indeed required for magnetic compass orientation in birds and salamanders. First evidence came from behavioral experiments with young homing pigeons that use their magnetic compass to record the direction of displacement: displaced in total darkness, they were disoriented (Wiltschko and Wiltschko 1981), just as young pigeons displaced in a distorted magnetic field had been (Wiltschko and Wiltschko 1978). Disorientation in the absence of visible light was also observed in the salamander Notophthalmus viridescens (Phillips and Borland 1992a). Later tests revealed a wavelength-dependency of the magnetic compass in amphibians (Phillips and Borland 1992b), migratory birds and pigeons (see Wiltschko and Wiltschko 2002). Marine turtles, on the other hand, proved well oriented in total darkness (Lohmann 1991; Lohmann and Lohmann 1993). Although an inclination compass is involved here, magnetoreception as proposed by the radical pair model appears unlikely, unless there is a yet unknown way that radical pairs could be generated in total darkness.
Demonstrating a radical pair mechanism
A diagnostic test based on magnetic resonance aimed at obtaining direct evidence for a radical pair mechanism underlying the avian magnetic compass. If the triplet yield is crucial for magnetoreception, interfering with the singlet-triplet interconversion should alter the output of the receptors markedly and thus disrupt magnetoreception. The singlet–triplet interconversion rate can be significantly affected by oscillating fields of specific frequencies in the MegaHertz range (Ritz et al. 2000). The intensities required for these resonance effects are so low that they would not affect any of the magnetite-based mechanisms currently considered (as explained below), so that a disruption of magnetic orientation would be diagnostic for the involvement of a radical pair mechanism.
At present, it is not easy to predict exactly which specific frequencies will interfere with the radical pair mechanisms underlying magnetoreception, because the chemical composition and the geometric structures of molecules involved are not yet known; theoretical considerations and in vitro studies indicate that they are to be expected in the 0.1–10-MHz range. The effect of the oscillating fields should depend on their orientation with respect to the static background field (Cranfield et al. 1994). These resonances are generally very broad and might therefore lead to disturbing effects at virtually all frequencies within this range, provided the intensity of the oscillating field is sufficiently strong (Henbest et al. 2004). However, a special resonance occurs when the frequency of the oscillating field matches the energetic splitting induced by the static geomagnetic field; here, one expects a marked effect regardless of the structure of the molecules forming the radical pairs. For the 46,000 nT geomagnetic field of Frankfurt, this frequency is 1.315 MHz (see Thalau et al. 2005).
Interactions of at least two receptors
If photopigments were involved, these pigments can hardly be expected to absorb light over the entire range of the visual spectrum – hence magnetoreception should depend on the wavelength of light. A wavelength-dependency of magnetic compass orientation was reported for salamanders, passerine birds, and homing pigeons. In the respective experiments, salamanders and birds were tested under monochromatic lights of various wavelength and intensities. By reflecting the absorption ranges of the crucial pigments, these studies may indicate the number of receptors involved and how they interact.
Salamanders show a wavelength dependency that is characterized by normal orientation only in a rather narrow wavelength band at the short-wavelength end of the spectrum and a variety of responses induced by long-wavelength light, with the specific manifestations of these responses attributed to different motivational stages. Salamanders manipulated to head shoreward showed normal orientation only up to 450 nm; at 475 nm, they were disoriented; and under wavelength of 500 nm and beyond, their headings were shifted by approximately 90° counterclockwise. When the animals were kept under long wavelength light with λ>500 nm, they showed a mirror-image clockwise shift under ‘white’ light, but headed shoreward under long-wavelength light (Phillips and Borland 1992b). To explain these findings, the authors suggested two antagonistic spectral mechanisms indicating directions perpendicular to each other. Only the short wavelength receptor was to indicate the correct magnetic directions, while the long-wavelength receptor activated by most of the visual spectrum indicated shifted ones. To reconcile these findings with the normal orientation observed under ‘white’ light, where both receptors are stimulated, the authors postulate that the signal of the short-wavelength dominates over the contradicting input (Phillips and Borland 1992b; Phillips et al. 2001). Since a spectral mechanism providing animals with false information is difficult to accept, Phillips and Deutschlander (1997) speculated about the two spectral mechanisms being connected, possibly being essential components of the same biochemical process.
When the salamanders were manipulated to head homeward, however, they were normally oriented only under 400 nm light and disoriented under wavelength of 450 nm and beyond (Phillips and Borland 1994). The authors attributed this disorientation to the false compass readings under long-wavelength light, which no longer allow the ‘map’-receptors to work properly and determine the home course. Held under long-wavelength light, the salamanders now preferred an axis that roughly corresponded with the magnetic north-south axis under both, ‘white’ and long-wavelength light (Phillips et al. 2002b). This response was discussed as being related to alignments and possibly controlled by tiny magnetite particles in the heads of the salamanders.
Most tests with birds used migratory orientation as a criterion whether or not normal directional information from the magnetic field could be obtained in a given situation. Migratory birds have not only been tested under different wavelengths, but also under different intensities and under combinations of two monochromatic lights. Their responses under the various light regimes indicate highly complex interactions between at least two, possibly more, receptors.
A second receptor with peak absorption at long wavelengths is also indicated by another finding. Although normally disoriented under long wavelengths, birds could orient under 645 nm red light after they had been exposed to this wavelength for 1 h prior to the critical test (Möller et al. 2001; Wiltschko et al. 2004a). The orientation induced this way proved to be normal migratory orientation. This ability to orient after having been pre-exposed to the test condition shows an interesting parallel to the ability to adjust the functional window to magnetic intensities outside the normal functional range (Wiltschko 1978) and may be based on similar mechanisms, namely learning to interpret a novel pattern of activation. The disorientation normally observed under red light suggests that under ‘white’ light, the long-wavelength receptor forms the minor component of a complex response pattern. Presented by itself, it would seem novel, but it would also be centrally symmetric to the axis of the field lines. Birds suddenly faced with this pattern alone might need a certain time until they are able to recognize its general characteristic and interpret it to derive magnetic directions (for a more detailed discussion, see Wiltschko et al. 2004b).
The nature of these odd responses is not yet clear. The axial preferences show some similarities to alignments, but unimodal tendencies in directions other than the migratory direction (e.g. Wiltschko et al. 2000, 2004b) are hard to explain. As motivational differences can largely be excluded, they imply that the magnetic receptors no longer provide information that can be used to locate the migratory course. Yet the light with identical spectral compositions, but lower intensity, allows excellent migratory orientation. The light levels of these brighter lights were still fairly low – on a sunny day, the natural light is brighter by powers of ten. Hence saturation of the receptors appears highly unlikely. Because ‘white’ light of high intensity allows normal orientation, the reason for the odd responses seem to lie in the near monochromatic nature of the light consisting of a narrow band of wavelengths only. Speculating on why this should matter leads to considerations about the interaction of the input of various receptors at higher centers. The number of receptors involved in magnetoreception is still unclear, but if they were more than one or two, monochromatic light would stimulate one receptor strongly, while others are not stimulated at all. This could result in an imbalance of input at higher units where the input of these receptors converge. The other receptors may also be specialized on magnetic input, or they may involve the cones of color vision which might provide background information of the general light level. Possibly, as long as the quantal flux is so low that the cones are not activated, monochromatic light from the blue-to-green part of the spectrum allows normal orientation; if the monochromatic lights are strong enough to activate the cones, however, the resulting imbalance might affect the processing of magnetic input in a way that the information content of magnetic input changes its general characteristics.
Bichromatic test lights: A combination of light from the blue-to-green part of the spectrum with 590 nm yellow light also leads to unimodal responses that no longer coincided with the natural migratory direction. These responses were likewise ‘fixed directions’, as they failed to show the normal seasonal change (Wiltschko et al. 2004b). The responses to bichromatic light combined from wavelengths where birds normally show excellent orientation, and yellow light, where they are disoriented when it is presented alone, clearly show that yellow light is not neutral, also pointing out interactions between at least two receptors that have not yet been fully understood. Interestingly, the specific response depended on the wavelength from the blue-to-green part of the spectrum: robins preferred northerly headings under green-and-yellow, southeasterly headings under turquoise-and-yellow and southerly headings under blue-and-yellow (Wiltschko et al. 2004b; Stapput et al. 2005). Apparently, the receptor(s) activated by light from the blue-to green part of the spectrum, although no longer providing magnetic compass information for locating the migratory direction, are active and determine the specific directions of the ‘fixed’ headings.
Similar patterns in birds and amphibians?
The findings described above indicate that certain light regimes drive the reception mechanisms for compass information towards their limits, leading to odd responses that cannot yet be explained. In birds, specific combinations of wavelengths as well as monochromatic light above a certain quantal flux result in such responses. To what extend this is also true for salamanders is unclear, because salamanders have not yet been tested under the same wavelengths at different intensities. It is interesting to note that the odd shifts in directions of salamanders heading shoreward and the disoriented behavior of salamanders heading homeward observed from 500 nm onward (Phillips and Borland 1992b, 1994; Phillips et al. 2002b) were recorded at light intensities where birds no longer prefer their migratory direction; at 400 nm, where salamander always showed normal orientation, the light intensity was markedly lower. Unfortunately, it is still unknown how salamanders would respond to long wavelengths at this lower light intensity. The manifestations of the responses under higher intensity – unimodal preference of unexplained directions, axial preferences and disorientation – are very similar in salamanders and birds. Hence it appears possible that the odd responses in these two animal groups represent related phenomena, which in salamanders depend not only on wavelength, as described by Phillips et al. and colleagues (e.g. 2001), but also on the intensity of light, reflecting a magnetoreception system functioning under borderline conditions. Future studies will have to clarify this question.
The site of the light-dependent magnetoreceptors
Another question concerns the location of the magnetoreceptors. Theoretical considerations favored the eyes as site of magnetoreception because of their almost spherical shape (Ritz et al. 2000) – this prediction has also been confirmed in birds, with the surprising finding that magnetoreception seems to be restricted to the right eye. Passerine migrants tested with their left eye covered were just as well oriented as binocular birds, whereas the same birds failed to show oriented behavior when their right eye was covered (Wiltschko et al. 2002a, 2003a). In salamanders, however, the receptors were found to be located in the pineal, the ancient third eye of vertebrates, which in amphibians is directly sensitive to light. Critical tests in which the skull above the pineal was covered with a color filter, but the eyes were open to the natural light, clearly showed that the magnetic compass in salamanders depended solely on the spectral properties of the light reaching the pineal (Deutschlander et al. 1999; Phillips et al. 2001).
Cryptochromes, first known from plants, but recently also discovered in animals (see Sancar 2003 for review) have been suggested to form the radical pairs involved in magnetoreception (Ritz et al. 2000). These photopigments have been found in the retina of vertebrates, first in mammals (Miyamoto and Sancar 1998), but also in chicken (Haque et al. 2002) and recently in migrating passerine birds. In Garden Warblers, Sylvia borin, cryptochromes are located in the large displaced ganglion cells (Mouritsen et al. 2004). In European robins, two forms of cryptochrome 1, splice product of the same gene, were identified, with the novel C-terminal of the second form implying a novel function (Möller et al. 2004). These findings support the idea that cryptochromes may be involved in the radical pair processes underlying the avian magnetic compass, yet direct evidence for their crucial role is still lacking.
Neuronal pathways associated with the avian magnetic compass
Our knowledge on the neural pathways and the parts of the brain processing magnetic compass information is rather limited; the available evidence comes entirely from studies with birds. Electrophysiological recordings in pigeons suggest that magnetic input is processed in parts of the visual system. Recordings from the nucleus of the basal optic root (nBOR) and from the tectum opticum revealed units that responded to changes in magnetic direction (Semm et al. 1984; Semm and Demain 1986). These responses are in accordance with the predictions of the radical pair model, as they were observed only in the presence of light; they seem to originate in the retina, as they depended on an intact retina and optic nerve. When the eyes were illuminated with monochromatic light of various wavelengths, units with a peak of responsiveness around 503 nm and others with a peak beyond 580 nm were identified, thus suggesting the two types of receptors with different absorption maxima, a finding that is in agreement with the behavioral studies likewise indicating two types of receptors with absorption peaks in the blue-to-green and in the long-wavelength range (e.g. Möller et al. 2001; Wiltschko et al. 2004b).
The finding that magnetic input is mediated exclusively by the right eye (Wiltschko et al. 2002a) indicates a stong lateralization of the magnetic compass that appears to be rather widespread among birds (see Wiltschko et al. 2003a; Prior et al. 2004). Because of the very few connections between the two hemispheres, it means that magnetic information is processed almost exclusively by the left hemisphere of the brain. This is intriguing, as a number of morphological asymmetries have been described in the tectofugal system, a part of the visual system (Güntürkün 1997) which, aside from the tectum opticum, comprises the nucleus rotundus, where activation by magnetic stimuli was indicated by the glucose method (Mai and Semm 1990). Together, the few findings available suggest that magnetic input originating in the right eye shares neuronal pathways with the visual system, being processed in the tectofugal system of the left hemisphere of the brain. Other parts of the brain involved in processing magnetic compass information are yet to be determined.
Magnetoreception based on magnetite, and associated findings
In the 1970s, certain bacteria were discovered to contain chains of single domain magnetite (Blakemore 1975) that act as magnets and align these bacteria along the field lines of the geomagnetic field. Magnetic information mediated by tiny magnets was an attractive idea, and the existence of magnetic material of biogenic origin caused authors to speculate about its potential role in the orientation of higher animals.
Based on theoretical considerations, the magnetite hypotheses propose a variety of models on how magnetite particles might mediate magnetic information, some of them involving single domains (e.g. Yorke 1979; Kirschvink and Gould 1981; Kirschvink and Walker 1985; Edmonds 1996), others superparamagnetic particles (e.g. Kirschvink and Gould 1981; Shcherbakov and Winklhofer 1999). A uniform concept on how magnetite-based magnetoreceptors might work does not yet exist. Interestingly, some of the models predict polar, others axial responses. Model calculations showed that magnetite-based receptors could convey directional information or information on magnetic intensity, depending on their specific structure and on the amount of magnetite included; they could account for the sensitivities indicated by behavioral evidence.
Magnetite has been discovered in a large number of species belonging to all major phyla, mostly by measuring the natural and induced remanence with highly sensitive SQUID-magnetometers. In honey bees, Apis mellifera, magnetic material was described in the front part of the abdomen (Gould et al. 1978); in vertebrates, it appears to be located mostly in the ethmoid region in the front of the head (see Kirschvink et al. 1985).
Effects of a strong, short magnetic pulse
The first behavioral tests were designed to generally demonstrate an involvement of magnetite in magnetoreception. They aimed at interfering with the potential receptors by altering the magnetization of the magnetite crystals. This was expected to change the output of receptors in a dramatic way and thus cause a lasting after-effect on orientation behavior. A popular method was to apply a brief, strong magnetic pulse to the head of the test animal – the pulse had to be strong enough to remagnetize the magnetite particles but, at the same time, short enough to prevent these particles from rotating into the pulse direction and thus to escape remagnetization. In most studies, a 0.5 T pulse with 3–5 ms duration was used.
Treating mammals with the same pulse also induced noticable deflections. Zambian molerats shifted the position of their nest by about 75° from the south-southeast to east. Retesting the same animals showed that this altered preference, in contrast to the one observed in birds, was stable for three months until the end of the experiments (Marhold et al. 1997b).
Single domains or superparamagnetic particles?
Since none of the other reception mechanisms would show an after-effect following treatment with a magnetic pulse, the observation that the pulse had an effect is diagnostic for magnetite particles involved in the receptor controlling the observed behavior. The response to pulse treatment can also be interpreted in view of the type of magnetite particles involved – single domains or superparamagnetic particles.
In birds, where both types have been described, the short duration of the pulse effect seems to speak against single domains. Remagnetization of single domain particles should be just as stable and lasting as the original one. Yet in birds, a clear pulse effect was observed only on the day of pulsing and the following two days (Wiltschko et al. 1994, 1998; Beason et al. 1997). The behavior of birds after pulse treatment thus indicates magnetite-based receptors, but these receptors do not seem to be based on single domains. This leaves superparamagnetic particles. Single superparamagnetic particles are not affected by a magnetic pulse as used in the experiments described above, but clusters and chains of clusters are. A strong pulse might break up the clusters and disrupt the chains, but they rearrange themselves, with a time rate in the order of several days, depending on the specific structure of the clusters, the angle with which they are hit by the pulse etc. (Davila et al., in press).
In rodents, the situation is different insofar as anatomical and histological data are entirely lacking. The pulse effect indicates a receptor based on magnetite, and the long duration of the pulse effect would be in accordance with single domains.
Neuronal pathways associated with magnetite-based receptors
Two other findings provide more direct evidence that the input from magnetite-based receptors in birds is mediated by the ophthalmic nerve: behavioral experiments showed that deactivating the ophthalmic nerve with a local anesthetic suppressed the pulse effect (Beason and Semm 1996); the bobolinks treated this way continued in their migratory direction, which clearly shows that the pulse does not affect the compass mechanism. In conditioning experiments, pigeons trained to respond to changes in intensity failed to respond correctly after deactivation of the ophthalmic nerve (Mora et al. 2004). Together, these findings suggest that in birds and probably also in fish, magnetite-based receptors mediate information on intensity rather than compass information.
In rodents, a study using c-Fos identified the superior colliculus as a site of neural activity caused by magnetic stimulation (Němec et al. 2001). The origin of this activity is unclear; an involvement of the magnetite-based receptor indicated by the pulse effect seems possible.
Two types of receptors for different tasks
In recent years, the number of publications on the aspects of reception and processing magnetic information has greatly increased, but it is only in case of birds, that the various pieces of the puzzle begin to form a consistent picture, although many questions still remain unanswered. The available data indicate the existence of two magnetoreceptor systems in birds for different types of information (see Beason and Semm 1991): a radical-pair mechanism in the right eye provides directional information, and magnetite-based receptors in the upper beak records differences in magnetic intensity – one might say: birds have a compass in their eye and a magnetometer in their beak. The input of the former appears to be mediated and processed by parts of the visual system, involving the nBOR, the tectum opticum and the nucleaus rotundus; the input of the latter by the ophthalmic nerve and the trigeminal ganglion. It is still unknown as to where these two types of information finally converge to form crucial components of the ‘map and compass’ system used for navigation (for review, see Wiltschko and Wiltschko 2003).
In other vertebrates, our knowledge is limited to certain aspects of magnetoreception. In marine turtles, the various uses of magnetic information are well documented, yet magnetoreception has not yet been analyzed. The nature of the primary processes of magnetoreception are indicated by behavioral data in salamanders, where the light-dependency of an inclination compass suggests magnetoreception based on a radical pair mechanism, and in mammals, where the pulse effect points to magnetite-based receptors. The position of the receptors and anatomical details about their structure are known in fish, where they are found in the olfactory lamellae; in salamanders, behavioral studies identified the pineal as site of the receptors. Some of the neuronal pathways are known in fish, where electrophysiological recordings indicate that information on magnetic intensity is mediated by the trigeminal system; in mammals, an involvement of the superior corniculus is suggested, but neither the origin nor the type of the respective magnetic information is entirely clear.
At the same time, the mechanisms employed by fish, mammals and several arthropods in their polarity compass are entirely unknown. Magnetite-based receptors are an option, as they could theoretically provide information on direction as well as on intensity. Here, the lasting pulse effect on nest building in mole rats is interesting: since the direction of the nest would involve only a compass, we may speculate that this compass might be based on single domain magnetite, but direct evidence is still lacking.
In view of the many open questions, we can only hope that the ‘magnetic sense’ continues to meet with great interest and that further research in the coming years will lead to a better understanding of reception and processing of magnetic information.