Magnetoreception in Mammals

CHAPTER TWO

Magnetoreception in Mammals Sabine Begall*,1, Hynek Burda*,†, Erich Pascal Malkemper*

*Faculty of Biology, Department of General Zoology, University of Duisburg-Essen, Essen, Germany † Faculty of Forestry and Wood Sciences, Department of Game Management and Wildlife Biology, Czech University of Life Sciences, Praha, Czech Republic 1 Corresponding author e-mail address: [email protected]

Contents 1. Biological Significance of Magnetoreception 2. How to Study Magnetoreception and Its Function in Mammals? Experimental Paradigms and Interpretation of Findings 2.1 Homing 2.2 Conditioning 2.3 Induced Analgesia in Mice 2.4 Resting Places in Rodents and Bats 2.5 Magnetic Alignment 3. Mechanisms of Magnetoreception in Mammals 3.1 Magnetite 3.2 Chemical Magnetoreception 3.3 Electromagnetic Induction 4. Do We (Humans) Sense the Magnetic Field? 5. The Impact of Anthropogenic Magnetic Noise on Mammals Acknowledgments References

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1. BIOLOGICAL SIGNIFICANCE OF MAGNETORECEPTION Magnets and magnetism have nowadays very wide technological application (e.g., storage of information on magnetic tape such as on audiocassettes, on magnetic strips on credit cards, in loudspeakers to convert electric energy into mechanical energy, in medicine for magnetic resonance imaging, and many more), however, most people associate those terms mainly with items which attract iron and with a compass. And although it appears that magnetic fields have also wider range of biological significance than previously thought (e.g., pain reception and circadian clocks to name Advances in the Study of Behavior, Volume 46 ISSN 0065-3454 http://dx.doi.org/10.1016/B978-0-12-800286-5.00002-X

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2014 Elsevier Inc. All rights reserved.

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just a few), researchers traditionally considered the compass principle as the major use of magnetism in animals. The ability to sense the geomagnetic field, in short magnetoreception, has fascinated (not only) researchers for almost half a century, starting when Wolfgang Wiltschko first provided evidence for its existence in a migratory bird (Wiltschko, 1968). Up to now, a number of species of most classes of vertebrates has been shown to possess a magnetic sense (Wiltschko & Wiltschko, 1995) but, contrary to general trends in biology, studies on mammals are still underrepresented in this field of research. Among vertebrates, not only birds but also teleosts, sea turtles, and amphibians have managed to attract more attention of researchers studying magnetoreception than mammals. Why particularly birds became the researchers’ favorite study subjects has historical and methodological reasons. Homing and navigation abilities of pigeons and migratory bird species have fascinated people for centuries, and research (including model species, experimental designs, etc.) on orientation and navigation in birds was established in many laboratories well before the role of magnetoreception was recognized and first proved. A comparable useful pool of study designs to draw on in magnetic research was not available for mammal species at that point. Although in mammals also long-distance migrations are known (whales, bison, caribou, East African gnus, etc.) and the homing abilities of dogs, cats, and horses are well (albeit only anecdotally) documented, experimental paradigms, such as the Emlen funnel and migratory restlessness (Zugunruhe) in birds, were not available for mammals. Displacement experiments with big mammals and homing experiments with cats, dogs, and horses are—for ethical and technical reasons—also not practicable. It was only until very recently that new methods and insights have emerged that enable us to study the distribution and nature of the magnetic sense on a broader scale. Humans find technical compass and GPS navigation systems useful for orientation also on a small scale (e.g., in forests or in the city), yet people usually still ask why animals like red deer, cattle, or the red fox should be magnetoreceptive if they do not migrate over long distances like some birds. However, unless an animal species has been specifically studied by radiotelemetry or by other adequate methods, and unless animals are not constrained by natural or artificial barriers, we usually cannot be sure whether individuals of the given species or population are indeed sedentary, vagrant, or migratory. In any case, we should emancipate ourselves from considering magnetoreception an exotic sense only because we, humans, do not have conscious intimate experience with it. The magnetic sense

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may be of use not only for long-distance migration, and not only for providing spatial (directional/compass and topical/map) information, but also in diverse other contexts of everyday life. Most evidence for the use of a magnetic sense in mammals has been so far collected (and searched for) in the context of spatial orientation. A magnetic compass sense in combination with a reference map would be useful for spatial orientation in long-distance migrants, and/or in territories and home ranges without distinct landmarks. Local signs informing an animal about its actual position within its home range may be visual, olfactory, or acoustic—and they may provide the animal with a cognitive map, which could be used as a reference for the magnetic compass sense. But a magnetic compass sense alone (i.e., without a map) could also be very helpful in a great variety of contexts. A magnetic compass could be used, for instance, to keep the course of digging in subterranean mammals or the course of swimming in aquatic mammals. It could be also expedient for keeping a common direction of grazing in gregarious animals (such as large herbivores), which is of importance in order to synchronize movement, avoid collisions and keep a “common escape direction,” and thus maintain herd cohesion (cf. Section 2.5). Magnetoreception could theoretically also be utilized in chronobiology. The natural daily variation of the magnetic field follows a certain time pattern and might provide, at least theoretically, a Zeitgeber to animals living in a monotonous, stable, uniform sensory environment deprived of light cues (i.e., day-and night-cycles). Thus, it could be employed, for instance, by mammals living underground or in the deep-sea to synchronize their daily activities. The magnetic sense might also be used to estimate the distance to a given goal. This seems especially plausible for a mechanism proposed to underlie magnetoreception that involves a light-dependent process occurring in specialized photoreceptors which allows the animal to visualize information provided by the geomagnetic field (GMF) (cf. Section 3.2). This hypothesis was first proposed by John Phillips and colleagues who exemplified it in the everyday scanning and orientation of the surroundings by rodents (Phillips, Muheim, & Jorge, 2010). If true, it suggests new horizons for the biological significance of magnetoreception. Based on the model of Phillips et al., the range-finder-hypothesis has been suggested as a possible basis for hunting ˇ erveny´, Begall, Koubek, success in the red fox (cf. Section 2.5; C Nova´kova´, & Burda, 2011) and the estimation of flight distance and/or slope (inclination, cf. Hart, Malkemper, et al., 2013), and could be also useful for jumping or gliding mammals inhabiting trees, cliffs, or rocks.

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Here, we review the current state of knowledge of magnetoreception in mammals and discuss the approaches and findings of studies so far published.

2. HOW TO STUDY MAGNETORECEPTION AND ITS FUNCTION IN MAMMALS? EXPERIMENTAL PARADIGMS AND INTERPRETATION OF FINDINGS 2.1. Homing Many mammals are able to return to their home range after being relocated, in some cases over hundreds of kilometers (Rogers, 1988; Schmidt-Koenig, 1965). The first evidence for a magnetic sense, however, stems from orientation experiments with small epigeic rodents. 2.1.1 Homing in Rodents The ability of some rodents to return to their home range after being experimentally displaced for up to hundreds of meters has puzzled researchers for a long time, but compass-map based navigation has mostly been rejected as an explanation in favor of simple landmark-based piloting strategies (reviewed in Joslin, 1977). The majority of these early studies used the simple approach of capture, displacement, and recapture (e.g., Gentry, 1964; Murie & Murie, 1931) or recording of vanishing directions after release (e.g., Bovet, 1971); but these did not yield insights into the sensory mechanisms involved and often ended in negative results since the animals simply aimed for the nearest shelter. A major breakthrough was achieved by a new study design that measured the directional preference in an arena after release at an unfamiliar site instead of measuring the homing success. Mather and Baker (1980) were the first to successfully demonstrate the functionality of such a design in European wood mice (Apodemus sylvaticus), showing that they were significantly oriented toward the capture site by measuring the time spent in each of the arms of a four-arm maze (orientation cage). In subsequent tests, the authors displaced the wood mice under different magnetic field conditions during the outward journey and again used a four-arm maze to demonstrate the involvement of a magnetic sense in the orientation behavior of the displaced mice (Mather & Baker, 1981). The hierarchical use of different senses and the dominance of the visual sense were also demonstrated as the mice used the magnetic sense only when vision was restricted. However, despite using a similar experimental set up, Sauve´ (1988) could not corroborate the homing abilities of A. sylvaticus.

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Karlsson (1984) used modified Emlen funnels (originally used for orientation experiments in birds) to successfully show homing orientation in the bank vole (Myodes glareolus) in the dark and without olfactory cues. Unfortunately, Karlsson did not perform critical experiments with artificially altered magnet fields to test for magnetic cues. August, Ayvazian, and Anderson (1989) followed a similar protocol as Mather and Baker (1981) to test displaced white-footed mice (Peromyscus leucopus) for their homing preferences; but instead of a four-arm maze, the authors used a circular arena. Since the white-footed mice concentrated their exploration activities under different magnetic conditions in the sector of the arena corresponding to their homing direction, the ability of magnetic orientation in another small rodent was demonstrated. However, in subsequent years interest in homing studies in rodents decreased, partly as a consequence of the inconsistency of their replicability (e.g., Sauve´, 1988) and partly owing to the introduction of new and more elegant experimental paradigms (cf. Section 2.4.1). In a set of experiments with blind mole rats (Spalax ehrenbergi), Kimchi, Etienne, and Terkel (2004) connected path integration with magnetic orientation. The authors used an artificial tunnel system consisting of a peripheral loop and eight radial tunnel segments leading to a round center box. The mole rats started their outward journey from the box at the periphery, and after they had covered a certain distance, they were lured to the center. Then, the animals should choose the shortest way back to the start box; but in half of the tests, the horizontal component of the geomagnetic field was shifted while the animals were still in the center. The tests demonstrated that blind mole rats use idiothetic cues for relatively short outward journeys and external magnetic cues when the distance covered during the outward journey is longer.

2.1.2 Bats Use a Sun-Calibrated Magnetic Compass Since the majority of bats are nocturnal, a magnetic sense would be highly beneficial, especially during long-distance foraging and migration (cf. Neuweiler, 2000). This assumption was supported by the discovery of magnetic material (magnetite) in the body of bats (Buchler & Wasilewski, 1982, 1985). Behavioral evidence for a magnetic sense was, however, not published until more than 20 years later. In 2006, Richard Holland and colleagues exposed big brown bats (Eptesicus fuscus) to a 90
shifted magnetic field for 90 min after being displaced for 20 km from their

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home roosts (Holland, Thorup, Vonhof, Cochran, & Wikelski, 2006). After release, the flying directions were assessed by means of radiotelemetry, revealing a shift in the experimental group corresponding to the shift of the north direction. These results suggest that the animals were calibrating their magnetic compass during the time of magnetic field exposure. The fact that the magnetic treatment was performed during the time around sunset, in combination with many of the misdirected bats finding their way back to the roost on the second day, suggests that bats possess a sun-calibrated magnetic compass. This was confirmed in subsequent experiments (Holland, Borissov, & Siemers, 2010). 2.1.3 Magnetoreception in Cetaceans A magnetic sense in cetaceans has been assumed for a long time. As many species are accurate long-distance migrants in such a featureless environment as the open sea, a compass sense seems indispensable. Experiments with whales, however, are difficult to accomplish, so again first evidence was indirect. Margaret Klinowska was the first to suggest that whales have a magnetic sensory system (Klinowska, 1983, 1985). She plotted whale stranding positions on magnetic maps of the coast of Great Britain and noted that the strandings were associated with areas with local magnetic minima. Plenty of further studies have confirmed and extended Klinowska’s initial work (Kirschvink, 1990; Kirschvink, Dizon, & Westphal, 1986; Klinowska, 1988, 1989, 1990; Walker, Kirschvink, Ahmed, & Dizon, 1992). It seems that cetaceans normally use the (N–S running) contour lines of the geomagnetic field (i.e., the marine magnetic lineation produced from sea floor spreading) as guidance during long-distance navigation and become misguided by the anomalies that lead them to the shallow waters near the coast, where they are trapped and more likely to strand. Some strandings have been related to solar storms causing anomalies in the geomagnetic field. Recently, Vanselow and Ricklefs (2005), using a long-term data set comprising stranding records of sperm whales around the North Sea for almost three centuries (1712–2003), found that sperm whale strandings were related to the length of the solar cycle: strandings occurred more often during cycles with a shorter length than the usual 11 years, being a proxy for an increase in solar energy flux. It should be noted, however, that the distribution of sighted free-ranging dolphins (Delphinus delphis) could not be related to any magnetic pattern (Hui, 1994).

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2.2. Conditioning One of the simplest but at the same time quite time-consuming paradigms involves training procedures where the animals are, for instance, required to learn the association between a magnetic stimulus and a reward (or the avoidance of punishment), to learn a training direction, or to discriminate between two magnetic fields. The first experiments using conditioning procedures were, however, not successful. For example, Bauer, Fuller, Perry, Dunn, and Zoeger (1985) were not able to train Atlantic bottlenose dolphins to respond to a magnetic stimulus in a series of conditioning experiments, and Madden and Phillips (1987) obtained negative results when trying to condition opossums (Monodelphis domesticus) and hamsters (Phodopus sungorus) to enter a specific arm of a four-arm maze that was indicated magnetically (artificially produced magnetic fields of Earth’s strength; see Section 2.4.1 for improved experimental designs). Roswitha and Wolfgang Wiltschko give a detailed account of the potential reasons for the long list of failures, and although the majority of the experiments to which they refer were conducted with birds, similar reasons may also apply to mammals (Wiltschko & Wiltschko, 1996). Assuming the tested animal has a magnetic sense, the reasons why conditioning experiments have failed may still be manifold. The main reason may be that the animal is not able to create a cognitive link between magnetosensory stimulation and the task to be learned, for example, because, in the most simple case, the animal does not use magnetic field cues to solve the given problem (e.g., search for food) under natural conditions. The solution might be to use classical (instead of operant) conditioning, an approach which, to the best of our knowledge, has not yet been tested in mammals. Another problem may be that the magnetic compass must be activated (switched on), for example, by certain “cornerstones,” moving over certain distance, etc., that is, by a more “natural” situation than that offered in the laboratory. Kimchi and Terkel (2001) showed that the blind mole rat (S. ehrenbergi) uses the magnetic sense to accomplish conditioned orientation tasks. On three consecutive days with five trials per day, the animals had learned a nonsymmetrical way through a complex labyrinth to receive a reward. In all animals, the time and the number of errors decreased over the course of the study. In trial 14, half of the blind mole-rats were tested in an artificially produced magnetic field (horizontal component reversed), while the other half remained under control conditions (GMF). The mean

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number of errors and the time the animals needed to accomplish the task was significantly higher in the experimental group compared to the control group, indicating that the animals do not simply rely on idiothetic cues when finding their way through a labyrinth but also on external magnetic cues (Kimchi & Terkel, 2001). In a similar experiment, Kimchi and colleagues (2004) trained blind mole rats to follow a relatively long and complicated path in a labyrinth. After the animals had learned the way, they were tested in the same labyrinth, but with the possibility to use many shortcuts. Animals tested under local geomagnetic field conditions chose significantly more often a correct shortcut, and accomplished the task significantly faster, than animals tested under shifted magnetic field conditions. Recently, John Phillips and his colleagues have tested C57BL/6 mice in a very elegant water-maze experiment to show that the mice can learn rapidly (in only two short training trials) to associate a submerged platform with a given training direction under different magnetic conditions (Phillips et al., 2013). After just two short training trials, the mice searched the platform significantly longer in the previously learned direction than in the other arms of the four-arm maze during testing. The authors argue that the success of this experiment might be connected with the absence of other cues and a situation in which reorientation is absolutely necessary for the animals. With respect to these new findings, it is interesting that it was already shown 20 years ago that a brief exposure to a 60 Hz magnetic field (0.1 mT, oriented N–S) increased the performance of meadow voles (Microtus pennsylvanicus) in a water-maze task (Kavaliers, Eckel, & Ossenkopp, 1993).

2.3. Induced Analgesia in Mice A new and very promising paradigm for studying magnetoreception in mammals was discovered originally in the land snail Cepaea nemoralis (Kavaliers & Ossenkopp, 1988; Prato, Kavaliers, & Thomas, 2000). The authors found that exposure to extremely low-frequency magnetic fields (ELF MF) could induce or reduce analgesia in the snails. Subsequently, the authors turned to laboratory mice and found a comparable effect: repeated daily exposure to a null magnetic field (1 h in Mu-metal chamber) resulted in a significant reduction of nociception as assessed by the hotplate-test (Prato, Robertson, Desjardins, Hensel, & Thomas, 2005). In follow-up studies, the authors reintroduced ELF MF during the daily sessions into the shielded

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environment to investigate which intensities were needed to abolish the analgesic effect. The astonishing results suggest a very high sensitivity of the mice to ELF MF being as low as 33 nT at 30 Hz (Prato et al., 2011, 2013). In addition, the effect was shown to be dependent on ambient light (Prato et al., 2009), a highly interesting finding which we will further discuss in Section 3.2).

2.4. Resting Places in Rodents and Bats 2.4.1 Nest-Building Preferences in Rodents When released into a circular arena, and given access to evenly dispersed tissue paper scraps and food, Ansell’s mole-rats (Fukomys anselli, in earlier papers denoted as Cryptomys hottentotus) will construct a nest, in most cases near or at the wall. Having a detailed look at this behavior of these hamstersized subterranean African rodents, Hynek Burda recognized that the positions of the nests of different individuals were not random but rather concentrated in the south and south-eastern part of the arena (Burda, 1987; Fig. 2.1A). Since visual landmarks were absent and the use of olfactory cues unlikely, Burda and colleagues started a series of experiments under different artificially produced magnetic fields (Burda, Marhold, Westenberger, Wiltschko, & Wiltschko, 1990; Marhold, Burda, Kreilos, & Wiltschko, A

B

C

mN

mN

+66° inclination

mN

+66° inclination

–66° inclination

Figure 2.1 Nesting preference of Ansell's mole-rats Fukomys anselli under different magnetic conditions. (A) Under undisturbed geomagnetic field conditions (inclination: +66
; intensity: 47,000 nT) Ansell's mole-rats prefer to build their nests in the southeastern sector of a circular arena (each dot represents one nest, N indicates geomagnetic north; dotted inner circle represents the 0.05-level of significance); (B) under magnetic field conditions with shifted polarity, the mole-rats prefer to build their nests in opposite direction. (C) Reversing the inclination by a pair of Helmholtz coils (inclination: 66
) did not affect the directional preferences of mole-rats. All experiments were performed in darkness; mN ¼ magnetic North. Modified from Marhold, Burda, et al. (1997) and Marhold, Wiltschko, et al. (1997).

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1997; Marhold, Wiltschko, & Burda, 1997). Changing the horizontal direction of the magnetic field led to a corresponding shift in nest position (Fig. 2.1B). By contrast, swapping the vertical axis of the artificial magnetic field did not affect the nest-building position (Fig. 2.1C). Thus, Marhold, Burda, et al. (1997) and Marhold, Wiltschko, et al. (1997) concluded that the compass of Ansell’s mole-rats depended on the polarity of the magnetic field and not on inclination as is the case in birds. Since the nest-building experiments yield consistent results also in complete darkness, the mole-rats’ polarity compass seems to be independent of light. This simple assay proved to be robust and quickly became the standard in behavioral research on rodent magnetoreception. It has been successfully employed in unraveling many details of the mechanisms of rodent magnetoreception (see Section 3.1), in yielding basic insights into neuronal correlates (Burger et al., 2010; Neˇmec, Altmann, Marhold, Burda, & Oelschlager, 2001) and also, importantly, to extend knowledge of the taxonomic distribution of magnetosensitivity. Recently, the nesting assay has been used to demonstrate a magnetic sense in two additional species of Bathyergidae, the silvery mole rat (Heliophobius argenteocinereus) and the giant mole-rat (Fukomys mechowii) (Oliveriusova´, Neˇmec, Kra´lova´, & Sedla´cˇek, 2012). Since silvery mole-rats do not build nests when strips of tissue paper are offered, the assay had to be adapted: instead of nesting position, the researchers analyzed sleeping position within the arena, monitored by a camera. Interestingly, the preferred direction of both species was approximately west and, thus, differed from that of F. anselli. The possible biological significance of this divergence will be discussed below. Blind mole rats (S. ehrenbergi) prefer to build their nests in the northeastern part of the arena, but there were significant differences between females (95
, p < 0.01) and males (32
, p > 0.05) (Marhold, Beiles, Burda, & Nevo, 2000). These results were not consistent with those of Kimchi and Terkel (2001), who used a slightly different assay. They allowed single blind mole rats to explore an eight-arm labyrinth for 2 days. After that, they noted in which of the chambers connected to each of the eight arms the blind mole-rats had established their nests and found that the chambers oriented in southern directions (and especially south-western direction) were more often chosen than those pointing to northern directions. The animals responded to an artificially produced magnetic field (reversed horizontal component) by shifting their nesting position accordingly. Similar results were obtained in complete darkness (Kimchi & Terkel, 2001).

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In contrast to the subterranean rodent species that show a spontaneous nest-building preference, similar studies with epigeic rodents, for example, the Siberian hamster (P. sungorus) or C57BL/6J mice (Mus musculus), have not revealed conclusive evidence for an innate direction preferred for nesting. Instead, the direction in which the tested animals built their nests within a circular arena corresponded with the direction of the dark side of the home cages in which the animals had previously been kept (Deutschlander et al., 2003; Muheim, Edgar, Sloan, & Phillips, 2006), indicating that the directional preference was learned (cf. Section 2.2). Schleich and Antinuchi (2004) could not find any indication of a magnetic sense in tuco-tucos (Ctenomys talarum), a South American subterranean rodent. They tested the tuco-tucos in a series of different experiments but obtained only negative results. Still, it cannot be concluded that a magnetic sense is absent. One explanation might be that the tuco-tucos use a potential magnetic sense on other occasions than those presented during the study (the authors recorded, for instance, the direction of the tunnel openings within a sand-filled arena). Additionally, the use of appropriate circular statistics (Batschelet, 1981), which is key to studies of spatial orientation, might have yielded more definitive insights. 2.4.2 Roosting Preferences in Bats One year after the first discovery of magnetoreception in the big brown bat (Holland et al., 2006; Section 2.1.2), a magnetic sense was confirmed in another bat species. Wang, Pan, Parsons, Walker, and Zhang (2007) recorded the preferred hanging positions of captured Nyctalus plancyi bats in a dark chamber. In the natural magnetic field, the animals predominantly occupied the northern end of their roosting basket. Changes in the magnetic field were followed by accompanying changes of sleeping positions. This assay, analogous to the nest-building experiments in rodents, allowed the researchers to test the animals repeatedly in a controlled manner and in this way to titrate the components of the magnetic field responsible for the behavioral changes (discussed in Section 4). So far, only these two of the more than 1000 known bat species have been shown to possess a magnetic sense.

2.5. Magnetic Alignment 2.5.1 North–South Oriented Herding of Cattle In our first study on magnetic alignment (MA), we showed that the axial body orientation of cattle (also of red and roe deer—see below) during

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ˇ erveny´, resting and grazing deviates significantly from random (Begall, C Neef, Vojtech, & Burda, 2008). Google Earth aerial pictures collected from different countries all over the world were used to demonstrate that cattle prefer to align their bodies along the North–South axis (Fig. 2.2A) (Begall et al., 2008, 2011; Slaby´, Tomanova´, & Va´cha, 2013). Cattle on tracks, or at feeder or water troughs, were not taken into account, and we calculated one mean vector per herd to avoid any statistical bias due to herding (i.e., we regard each herd as a statistically independent entity). That this N–S-preference depends on the field lines of the geomagnetic field rather than on other cues is supported by several findings. First, the geomagnetic North–South axis is a better predictor for body orientation of cattle on pastures at locations with high negative and high positive declination values than the geographic North–South axis. Second, cattle under or near power lines (producing extremely low-frequency alternating magnetic fields) show a random distribution of their body axes, and body orientation becomes more N–S aligned the further the cattle are away from the power lines ˇ erveny´, Neef, & Neˇmec, 2009). The typical N–S align(Burda, Begall, C ment is shown at a minimal distance of approximately 150 m from the power lines, thus, we set a distance of at least 200 m for the “control conditions.”

Figure 2.2 Axial data revealing the N–S alignment in three ruminant species. (A) Cattle. (B) Roe deer. (C) Red deer. Each pair of dots (located on opposite sites within the unit circle) represents the direction of the axial mean vector of the animals’ body position at one locality. The double-headed arrow indicates the mean vector calculated over all localities of the respective species. The length of the arrow represents the r-value (length of the mean vector), dotted circles indicate the 0.01-level of significance. Triangles positioned outside the unit circle indicate the mean vectors of the cattle data subdivided into the six continents (dotted: North America; gray: Asia; checkered: Europe; striped: Australia; black: Africa; white: South America) (A) and the mean vectors of resting (black) and grazing (white) deer, and of deer beds (dotted) (B: roe deer; C: red deer). Modified from Begall et al. (2008).

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Hert, Jelinek, Pekarek, and Pavlicek (2011) have challenged the results of our original study (Begall et al., 2008) and claimed that cattle do not align their body in a North–South direction. However, it turned out that their methods were highly flawed: about 50% of their data represented noise (e.g., the resolution of the images was too poor to enable unambiguous measurement of the direction of body axes; hay bales or sheep were misinterpreted as cattle; pastures were on slopes, near settlements or highvoltage power lines, etc.), and the authors had selected only approximately 40% of cattle that were present on the pastures analyzed. Our reevaluation of the Google Earth aerial pictures collected by Hert and colleagues confirmed the original results and conclusions our team had drawn (Begall et al., 2011). The reanalysis also revealed that MA is more pronounced in lying/resting cattle than in standing/grazing cattle. Slaby´ and colleagues replicated the study of MA in cattle by means of Google Earth aerial snapshots. They also refined the evaluation method by using a blinded protocol, that is, without knowledge of the north direction during the measurements; and they included further restrictions, for example, only herds of cattle with more than 10 animals were evaluated and pastures had an elevation of less than 5 m over 100 m in any direction (Slaby´ et al., 2013). All in all, they confirmed our previous results. Furthermore, they measured the distance between individual cattle within a herd and showed that the alignment behavior is dependent on herd density (number of animals per 1000 m2). In herds with low density (approximately less than six animals per 1000 m2), axial mean vectors of both individual body orientation and mean orientation calculated per herd deviated highly from random orientation, with a preference for N–S direction. In herds with medium density (more than 6 animals but less than 12 animals per 1000 m2), only the axial mean vector calculated over individuals (but not over mean vectors of herds) showed a significant alignment along the N–S axis. Body orientation of cattle kept at higher densities (more than 13 cattle per 1000 m2, corresponding to a distance of approximately 6–8 m or even less between individuals) was random. Thus, the authors argued that MA might be masked by social interactions in high-density herds (Slaby´ et al., 2013). They also stressed the problematic definition of a herd, since dense herds, as are typical for Europe, might not be comparable to the widely scattered herds of North America. Thus, Slaby´ and colleagues suggested it might be worth considering an individual within a scattered herd as an appropriate (i.e., statistically independent) unit rather than a whole herd. The biological meaning of the phenomenon is still enigmatic and will be discussed below.

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2.5.2 Magnetic Alignment of Deer We recorded the body position of 2974 deer at 227 localities in the Czech Republic to study alignment of red deer (Cervus elaphus) and roe deer (Capreolus capreolus). We used direct snapshot observations of grazing/resting deer and recordings of deer beds (i.e., body prints of resting animals in the snow or on the ground). The analysis revealed that axial body orientation of red deer and roe deer show a significant deviation from random distribution (Fig. 2.2B and C) and, as in cattle, deer align their body axis in approximately N–S direction. The direct observations also allowed us to differentiate between the head and the rear of an animal, so we were able to analyze angular data as well. The circular statistics showed a bimodal distribution with a preference for magnetic north compared to magnetic south, that is, the majority of grazing and resting deer face northward (Begall et al., 2008). Similar to the findings for cattle, roe deer are randomly oriented in the vicinity of power lines (Burda et al., 2009). 2.5.3 Mousing Behavior of the Red Fox Our finding that cattle and deer align their body axis approximately along the field lines of the geomagnetic field led us to inspect different behaviors of different species more closely. We investigated (among others) the mousing of red foxes, which is a specific behavior shown during hunting of small mammals. The fox approaches its prey carefully and slowly to avoid making noise; it stops at a certain point; then it jumps high in the air and virtually attacks its prey from above. Jumping directions were determined by direct observation (23 experienced wildlife biologists and hunters provided independent recordings). The direction in which red foxes jump during mousing ˇ erveny´ et al., 2011): circular analysis is significantly different from random (C of the angular data (head direction of jumps) revealed a significant preference for NE. Since this preference was independent of the observer, time of day, season, wind direction, etc., we propose that the mousing behavior is another case of alignment with respect to GMF. Interestingly, red foxes mousing in high cover (i.e., when the prey is hidden in high vegetation or under snow cover), where visually guided attacks are not possible, had higher hunting success when the jumps were oriented toward north (segment: 340–40
; 72.5% hunting success) or south (160–220
; 60% hunting success) compared to other directions (success rate in other segments less than 18%) (Fig. 2.3). Here, approximately 82% of all successful jumps were directed toward N or NE. Unsuccessful jumps were more scattered. By contrast, red foxes mousing in low cover can spot their

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Figure 2.3 Hunting success of red foxes. The hunting success of mousing red foxes is dependent on the direction of the jumps with respect to the GMF lines. When vision is obstructed by snow or high vegetation, jumps from south–southwest and from north– northeast directions are much more successful than from other directions (percentage of successful jumps given in each sector; calculation based on 200 observed fox mousing jumps). Congruently, the foxes prefer to jump from these directions (shaded sectors) in high cover. Data from Červený et al. (2011).

prey visually and might not necessarily rely on aid from the field lines of the geomagnetic field. Accordingly, the mousing jumps in low cover ˇ erveny´ et al., 2011). The sensory aspects showed high directional scatter (C of this peculiar behavior can be explained by the so-called “range-finderhypothesis,” which provides a theoretical basis for the differential hunting success in dependence of the MA of the red fox and is described ˇ erveny´ et al. (2011). In short, the hypothesis proposes in detail in C a direction-dependent improvement of target–distance estimation by the fox, mediated by a photoreceptor-based magnetoreception system (cf. Section 3.2).

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For a detailed description of the methods used in these studies and a discussion of MA in mammals and other animals, see Begall, Malkemper, ˇ erveny´, Neˇmec, and Burda (2013). C 2.5.4 Dogs Sense Small Changes in the Rate of Declination Recently, we found that also dogs show MA under certain conditions (Hart, Nova´kova´, et al., 2013). We measured body orientations of 70 dogs of different breeds while they were off-leash in the open country during territorial marking (urination, 5582 observations) and defecation (1893 observations). The analysis of all events revealed no preference for any specific direction. However, when we sorted the data according to the geomagnetic conditions prevailing during the respective sampling periods, a clear picture emerged: The dogs preferred to align their bodies during marking and excretion along the magnetic North–South axis only under calm magnetic conditions, more specifically when the declination was stable. We speculate that the dogs possess a mental map of their home range and recall it whenever being in unfamiliar regions. They might store the location (coordinates) of marking cornerstones in their memories and/or use such short stops to recalibrate their magnetic compass and/or compare their cognitive maps with the actual landscape. This is probably easier when being aligned with the magnetic field and under calm magnetic conditions.

3. MECHANISMS OF MAGNETORECEPTION IN MAMMALS Receptors for the detection of magnetic fields have not yet been conclusively demonstrated in any animal. However, findings from behavioral, histological, and electrophysiological studies have led to several physically viable conjectures that might also apply to mammals. Here, we focus on the three most supported and most vividly discussed mechanisms: a magnetite-based mechanism, the radical-pair mechanism, and electromagnetic inductions. Several other mechanisms, such as induced fluid streaming (Bamberger, Valet, Storch, & Ruhenstroth-Bauer, 1978) and cyclotron resonance (Liboff & Jenrow, 2000) have been suggested, but since they have not received substantial support from behavioral experiments, we do not consider them in this review.

3.1. Magnetite Perhaps the most intuitive (at least to the human imagination) mechanism to explain magnetosensitivity in animals is the idea of a small permanent

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magnet inside the animal that acts like a compass needle (Yorke, 1979). It is therefore not surprising that after the initial discovery of biogenic magnetic material in the teeth of chitons (Lowenstam, 1962) and the subsequent demonstration of magnetite (Fe3O4) chains and their crucial role in the magnetotactic behavior of certain bacteria (Blakemore, 1975; Frankel, Blakemore, & Wolfe, 1979), a rigorous search was performed to map the distribution of this new biogenic material. Within a period of less than 20 years, suitable magnetic particles were demonstrated in different tissues of a variety of animals. The occurrence of these ferrimagnetic particles in rodents (Mather, 1996), bats (Buchler & Wasilewski, 1982), marine mammals (Bauer et al., 1985; Zoeger, Dunn, & Fuller, 1981), and even humans (Kirschvink, Kobayashi-Kirschvink, & Woodford, 1992) makes it tempting to speculate that magnetite is a common mammalian feature and perhaps serves a magnetoreceptive function. Indeed, it has been speculated that a magnetic sense based on magnetite evolved so early in animal history that it is a common feature of all animal phyla (Kirschvink, Walker, & Diebel, 2001). Consequently, the theory of a magnetite-based mechanism of magnetoreception has found general acceptance today even though many details are still unknown (Kirschvink, Winklhofer, & Walker, 2010; Wiltschko & Wiltschko, 2012b). In general, two different types of magnetite particles suitable for an animal magnetoreceptor can be distinguished: larger (>50 nm) particles are called single-domain (SD) particles and possess a permanent magnetic moment, while smaller superparamagnetic (SPM) particles (3–5 nm) obtain their magnetic moment from an external magnetic field (Kirschvink & Gould, 1981; Kirschvink & Walker, 1985). Theoretically, both particle types might constitute an animal magnetoreceptor either independently or arranged as hybrid detectors (Davila, Fleissner, Winklhofer, & Petersen, 2003; Kirschvink & Gould, 1981; Solov’yov & Greiner, 2007), and both types have been found to occur in animal tissues (e.g., Diebel, Proksch, Green, Neilson, & Walker, 2000; Hanzlik et al., 2000; Walcott, Gould, & Kirschvink, 1979). Still unsolved, however, are questions about how the magnetic stimulus is transduced into nerve signals and where exactly the receptors are located. Nerve cell excitation is always accomplished by transient changes in the conductivity of nerve cell membranes. There are several possibilities as to how ferromagnetic particles might accomplish this task. With respect to the size and magnetic properties of the particles found in animals, two hypotheses about the transduction mechanism are widely acknowledged

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by the scientific community. The first hypothesis states that SD magnetite, either alone or in combination with SPM agglomerations, is embedded in the cell membrane. Presuming that these particles are partially electrically isolated and/or elongate, an interaction with an external magnetic field will alter their orientation and thus directly modify the electron conductivity of the membrane (Fig. 2.4A; Kirschvink & Gould, 1981). Due to the fact that nerve cells are generally excited by the opening/closing of ion channels and the movement of ions rather than just electrons, a second theory of the transductive mechanism has received stronger support. This theory is that cytosolic or actin filament anchored SD-magnetite chains control ion channels either directly via a torque mechanism or indirectly through membrane deformation (Fig. 2.4B and C; Kirschvink & Gould, 1981; Winklhofer & Kirschvink, 2010). Based on histological findings in pigeons, a direct coupling of magnetite particles to highly sensitive muscle spindles has also been suggested (Presti & Pettigrew, 1980) but this mechanism has not gained further evidence so far. Yet another mechanism for magnetite magnetoreception has been proposed by Edmonds (1996). According to his idea, a group of SD-magnetite particles is embedded in a liquid crystal of a photoreceptor. Within this crystal, the SD-particles will be able to rotate freely and align with superimposed magnetic fields. The model further assumes that the liquid crystal also contains dye molecules with anisotropic absorption (e.g., carotenoids), which means that they absorb light only under a specific angle of incidence. The oil droplets that are found in the cones of some birds and reptiles fulfill these requirements (Edmonds, 1996; Goldsmith, Collins, & Licht, 1984). With this arrangement of magnetite and pigments, light of the wavelength-band absorbed by the pigment would only reach the photoreceptor when the cone is aligned parallel or antiparallel to the magnetic field lines. Many behavioral findings on magnetoreception in birds, such as its strong wavelength dependency (Wiltschko & Wiltschko, 2001), could be explained by the liquid crystal mechanism. However, so far it lacks one crucial aspect: magnetic particles have not been found in oil droplets. Furthermore, within the scope of this review the mechanism seems even more unlikely, since mammalian cones do not possess oil droplets (Kelber, Vorobyev, & Osorio, 2003). For mammals, aside from the detailed realization of the transduction mechanism, a bulk of behavioral and histological data support the involvement of ferromagnetic particles in the magnetic sense. Firstly, as mentioned above, magnetite has been demonstrated to occur in many mammals, but this finding alone does not prove anything about its significance.

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Figure 2.4 Three suggested models of the cellular signal transduction in a magnetitebased mechanism of magnetoreception. (A) The membrane-short model. An elongated magnetite particle is embedded in the cell membrane. The particle is partially isolated (black layer) and aligns within a superimposed magnetic field. Only in a certain alignment, the particle creates an electric shortcut which leads to de- or hyperpolarization of the cell. (B) The torque-transducer model. A chain of SD-magnetite particles is anchored at the cell membrane. The tip of the chain is connected to several gaiting filaments, which control the flow of intermembrane ion channels (note that only one channel is exemplified in the figure). Depending on the direction of the magnetic field, the chain is variably deflected and opens ion channels while closing others, ultimately changing the membrane potential. (C) The membrane deformation model. A magnetite cluster exerts a pressure on the cellular membrane and deforms it in a manner that is dependent on the alignment of the cluster with respect to an external magnetic field. The deformation directly opens or closes ion channels. The figure is not drawn to scale. (A) After Kirschvink and Gould (1981); (B) after Walker, Dennis, and Kirschvink (2002) and Winklhofer and Kirschvink (2010); (C) after Solov’yov and Greiner (2007).

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An SD-magnetite magnetoreceptor enables an animal to perceive the polarity of the magnetic field and is insensitive to low-intensity oscillating magnetic fields in the MHz range (radiofrequency; RF). In contrast, RF magnetic fields do interfere with radical pairs (Henbest, Kukura, Rodgers, Hore, & Timmel, 2004; Ritz, Thalau, Phillips, Wiltschko, & Wiltschko, 2004), thus disabling a radical-pair mechanism (see Section 3.2). In addition, SD-magnetite receptors have a unidirectional permanent magnetic moment and their polarity can be flipped by a short but strong magnetic pulse (Kalmijn & Blakemore, 1978). Each of these intrinsic and delimiting properties can be exploited in behavioral experiments to determine whether magnetite receptors are involved. The first experimental paradigm that yielded replicable, reliable results, and thus could be used to investigate the properties of the magnetoreceptor in a mammal, was the nest-building assay with mole-rats of the genus Fukomys (cf. Section 2.4.1). When mole-rats were treated with a strong magnetic pulse prior to testing, they changed the direction of their nestbuilding preference by 90
, an effect that lasted for several weeks (Marhold, Burda, et al., 1997). A long-lasting effect of pulse treatment is in accordance with the SD character of magnetite particles—but since no recovery from the effect was reported in the mole-rat experiment, unspecific effects on the receptors cannot be ruled out. However, the same authors showed that mole-rats respond to the polarity of the magnetic field rather than to its inclination (Marhold, Burda, et al., 1997; Marhold, Wiltschko, et al., 1997); and both of these findings combined strongly suggest the involvement of SD-magnetite. Sensitivity to the polarity of the magnetic field was subsequently demonstrated in another subterranean rodent species, the blind mole-rat S. ehrenbergi (Kimchi & Terkel, 2001). Two epigeic rodents, the Siberian hamster P. sungorus and laboratory C57Bl6/6J mice, have also shown clear magnetic orientation but the experiments performed so far do not allow any conclusive statement about the underlying receptor mechanism (Deutschlander et al., 2003; Muheim et al., 2006, but see Section 3.2). The latter is also true for the controversial homing experiments on the European wood mouse (Mather & Baker, 1981). Even though pulsing experiments had indicated magnetite as the basis of magnetoreception in mole-rats, it took almost 10 years until the possible localization of the magnetoreceptor cells was shown by an elegant combination of histological and behavioral investigations. Here, in spite of the fact that the subterranean mole-rats have strongly reduced eyes, iron staining

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(Prussian blue) revealed small particles in the corneal epithelium (Wegner, Begall, & Burda, 2006). Congruently with an involvement of these particles in magnetoreception, corneal anesthesia abolished the natural preference of the animals to build nests in the south-eastern sector of a circular arena. As opposed to sham-treated control animals, the nests of the anesthetized animals were randomly distributed even though the visual sense was not impaired by the treatment (Wegner et al., 2006). In agreement with comparable impairment of magnetoreception in beak-anesthetized birds (Wiltschko, Munro, Ford, & Wiltschko, 2009), these findings on the cornea constitute the best evidence for the seat of the mammalian magnetoreceptors so far. Moreover, the mammalian cornea is innervated by the trigeminal nerve, which has also been proposed to carry sensory information from (magnetite-based) magnetoreceptors in birds (e.g., Heyers, Zapka, Hoffmeister, Wild, & Mouritsen, 2010; Mora, Davison, Wild, & Walker, 2004, but see Treiber et al., 2012; Wu & Dickman, 2012). Finally, neuronal activation studies in mole-rats revealed magnetic field-dependent activity in a layer of the superior colliculus that dominantly receives trigeminal input (Neˇmec et al., 2001). Bats, the only group of nonrodent mammals studied in this respect so far, also use a polarity compass rather than an inclination compass (Wang et al., 2007). In accordance with this, pulsing also disrupted the homeward orientation of displaced big brown bats E. fuscus (Holland, Kirschvink, Doak, & Wikelski, 2008). To sum up, magnetite-based magnetoreception is a highly promising candidate in mammals. All species that have been specifically tested so far responded to the polarity of the magnetic field and are disturbed by magnetic pulses but not by weak RF fields (see below). However, this should not be taken as an argument against other mechanisms, since the existence of one receptor mechanism does not rule out the involvement of others. In birds, it is generally accepted that magnetite receptors are complemented by a chemical magnetoreceptor mechanism, most probably located in the eye (cf. Section 3.2), with the two mechanisms being used in different tasks (Wiltschko & Wiltschko, 2012a). Two distinct magnetoreceptors have also been found in amphibians (Phillips, 1986).

3.2. Chemical Magnetoreception More recently another mechanism for magnetoreception in animals has been proposed (Ritz, Adem, & Schulten, 2000), which goes down to the

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quantum mechanical level of a chemical reaction and requires radical pairs. It is widely accepted that these radical pairs are produced by a light-sensitive molecule that changes its oxidation state after photoexcitation and that this reaction most likely takes place in the retina (Ritz, Ahmad, Mouritsen, Wiltschko, & Wiltschko, 2010). The observation of a physiochemical interaction between radical pairs and weak magnetic fields and its putative use in biomagnetic sensors was published years before theories of magnetite magnetoreception were formulated in detail (Leask, 1977; Schulten, Staerk, Weller, Werner, & Nickel, 1976; Schulten, Swenberg, & Weller, 1978). These early considerations, however, suffered from several intrinsic requirements that were not met by any known biological molecule. Therefore, it was not until the beginning of this century that the idea was reassessed and a coherent and plausible theory of chemical magnetoreception in birds was formulated (Ritz et al., 2000). The mechanism proposed by Ritz and colleagues (2000, 2010) requires that a donor molecule is excited by light and consequently transfers an electron to a nearby acceptor molecule (Fig. 2.5A). In the following intermediate state of the reaction, both molecules possess an unpaired electron, thus forming a radical pair (Fig. 2.5B). The free electrons of the radical pair switch between two different spin states, the singlet (antiparallel spin) and triplet (parallel spin) state. These spin states are basically small magnetic moments and they can be influenced by external magnetic fields (Fig. 2.5C). If an external magnetic field is applied, the interconversion between the two spin states is dependent on the alignment with, and the general intensity of, the magnetic field. In the final step (Fig. 2.5D), the radical pairs react and form distinct products for each of the intermediate states. Ultimately, the yield of triplet products allows the animal to extract information about the intensity of the magnetic field and the alignment of the receptor molecules with respect to the magnetic field lines. In particular, the critical transition between the spin states can be specifically affected through resonance effects with weak (nT-range) oscillating magnetic fields in the range between 0.1 and 10 MHz, a property that can be utilized as a diagnostic tool in behavioral experiments (Ritz et al., 2004). Cryptochrome, a blue-light sensitive photoreceptor molecule, is at present the most promising candidate for the magnetoreceptor (Liedvogel & Mouritsen, 2010; Ritz et al., 2000, 2010). It is present in retinal cells of a variety of plant and animal species, including mammals, where it is known to be responsible for the maintenance of circadian rhythms (Cashmore,

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Figure 2.5 A simplified mechanism of the radical-pair mechanism of magnetoreception. (A) A donor molecule (D) is excited by light (of specific wavelengths) and subsequently transfers an electron to a nearby acceptor molecule (A). (B) This leads to the generation of a radical pair where both molecules possess a single unpaired electron. (C) The unpaired electrons of both radical-pair partners can exist in two different states (singlet and triplet). Depending on the intensity and direction of an external magnetic field, the interconversion between the states is shifted to one direction. (D) The switching state of the radical-pair spin state leads to varying yields of respective products. The comparison of the product yield enables the animal to extract information about the parameters of the magnetic field. Modified from Ritz et al. (2009).

Jarillo, Wu, & Liu, 1999; van der Horst et al., 1999). The orbital arrangement of the retinal cells fulfills a critical prerequisite for the radical-pair compass to work: the cryptochrome molecules of the different cells are aligned into distinct directions (Ritz et al., 2000). If we further assume that within any sensory cell the alignment of the cryptochrome molecules is uniform, the triplet product yield at any given moment will vary across the retina. This pattern is believed to be perceived by the animal as a light-dark pattern superimposed on the normal visual scene (Ritz et al., 2000; Solov’yov, Mouritsen, & Schulten, 2010). The pattern is complex but axially symmetrical, which means that if an animal is looking parallel to the field lines it cannot distinguish between “looking north” and “looking south.” This is in accordance with the behavior of migratory birds, which also do not respond to a change in the polarity of the magnetic field but rather to its inclination (Wiltschko & Wiltschko, 1972). The description of the radical-pair mechanism given above is a rather simplified and general version of a very complex model. The simplification was chosen on the one hand in consideration of the scope of this review but also and importantly because many basic parameters of the reaction

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mechanism are still unclear. For example, it is not resolved what exactly is the signaling state of cryptochrome in animals (Nießner et al., 2013), which radical pairs are involved and essential for magnetoreception (Mu¨ller & Ahmad, 2011; Ritz et al., 2009), which anisotropy accounts for the directional sensitivity of the radical pair (Lambert, De Liberato, Emary, & Nori, 2013), or whether the chemical or physical properties of the radical pair are responsible for the sensation (Stoneham, Gauger, Porfyrakis, Benjamin, & Lovett, 2012). In mammals, no direct evidence for the use of a radical-pair-based mechanism of magnetoreception exists so far. For mole-rats, in addition to the above-mentioned findings that indicate a magnetite magnetoreceptor (pulse effect, response to polarity), experiments with RF oscillating fields did not affect the directional preference in the nest-building assay (Thalau, Ritz, Burda, Wegner, & Wiltschko, 2006). This indicates that mole-rats either do not possess a light-dependent radical-pair-based magnetoreceptor, which would make sense in a lightless subterranean environment (cf. Wegner, Burda, Begall, & Neˇmec, 2007), or that they do not use it in the nestbuilding task. For epigeic rodents, there are some indirect clues that hint toward the existence of a radical-pair-based magnetoreceptor. The first is related to the complexity and the axial symmetry of the visual pattern that is assumed to be created by the retinal magnetoreceptors. Mice that were trained to build their nests in one of the four cardinal magnetic directions behaved differently when they were trained to build in N or S than when they were trained to build in E or W. While the nests of N–S mice were clustered in the trained direction, the nests of E–W mice formed two distinct clusters centered around the trained direction (Muheim et al., 2006; Painter, Dommer, Altizer, Muheim, & Phillips, 2013). This discrepancy suggests the perception of a complex pattern, rather than a simple compass direction (Painter et al., 2013). Further indirect evidence for the involvement of radical pairs in mammal magnetic orientation stems from very recent findings of mouse water-maze experiments. As already described in Section 2.2, mice in a water-maze task can quickly be trained to search for a hidden platform in a specific magnetic direction (Phillips et al., 2013). Yet, before these elegant experiments yielded stable results, the authors had to struggle with a variety of confounding factors. One of these factors were RF fields between 0.2 and 200 MHz, which had to be significantly lowered inside the test buildings for the mice to be reliably oriented (Phillips et al., 2013). The authors state

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that these precautions were also crucial for the experiments on mice and hamster nest-building published earlier (Deutschlander et al., 2003; Muheim et al., 2006; Phillips & Deutschlander, 1997; Phillips et al., 2013). If the mice were using a magnetite-based mechanism for these tasks, the weak RF magnetic fields that are typical of laboratory environments would not have had any effect. Adding to these findings of RF-sensitivity are the experiments by Prato and colleagues with CD-1 mice. The effect of low-frequency magnetic fields on nociception (cf. Section 2.3) was shown to be clearly dependent on the ambient light regimes during the treatment (Prato et al., 2009). Broad spectrum (400–750 nm) and UV light induced the effect, while red light did not, and under blue light the effect depended clearly on intensity. These light regimes match the absorbance spectrum of cryptochrome and the behavioral effects are comparable to observations on orientation and disori˚ kesson, 2002; Wiltschko, Munro, entation in birds (Muheim, Ba¨ckman, & A Ford, & Wiltschko, 1993). Early experiments on pineal physiology that indicate involvement of the retina in rodent magnetoreception extend the line of evidence (reviewed in Olcese, 1990). A single 30-min change in the ambient magnetic field during the night resulted in a depression of pineal melatonin synthesis in rats (Welker et al., 1983). This effect was abolished when the rats’ optic nerves were cut before the MF treatment, thus indicating retinal involvement (Olcese, Reuss, & Vollrath, 1985). A later study confirmed that this effect was indeed light dependent as rats kept under dim red light were sensitive to the effect, in contrast to rats kept in total darkness (Reuss & Olcese, 1986). Interestingly, the MF effect was also abolished by degeneration of the outer segments of the rat photoreceptors (Olcese, Reuss, Stehle, Steinlechner, & Vollrath, 1988), a region which in birds contains activated cryptochrome 1a under influence of light of specific wavelengths, such that it strongly suggests its involvement in magnetoreception (Nießner et al., 2011, 2013). Yet the results in rats remain puzzling since, even though they prove the light dependency of the MF effect, they are not consistent with the behavioral results in migratory birds, which were disoriented in dim red light of comparable intensity (Wiltschko et al., 1993). The presence of a cryptochrome-based system that mediates magnetosensitivity via two antagonistic channels, as has been proposed for amphibians by Phillips and Borland (1992), might resolve this inconsistency. At least on a theoretical level, the observations are also explicable with a receptor based on magnetite particles suspended in nematic liquid crystals as proposed by Edmonds (1996), if

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suitable liquid crystals could be found in mammalian retinae. Finally, doubts have been raised about the magnetosensitivity of the pineal gland in the rat experiments, since the effects are most likely the result of induced currents through the rapid switching of the magnetic field (Lerchl, Nonaka, & Reiter, 1991). However, this does not rule out the possibility that retinal magnetoreceptors were the site of action (Phillips & Deutschlander, 1997). To summarize, it is still unclear whether or not a radical-pair-based mechanism is used in mammalian magnetoreception. Further behavioral and physiological experiments should primarily address the effects of RF fields and different light wavelengths as well as darkness on mammal magnetoreception, especially on epigeic rodents. RF fields will have to be shielded and then reintroduced into the test environment, allowing determination of the exact frequencies and minimal intensities needed. In addition, future studies should make precise distinctions between different behavioral tasks to determine whether effects are context dependent. For example, this might reveal a division of labor between radical pair and magnetite receptors as has been proposed in birds (Wiltschko & Wiltschko, 2007). Thus, it seems reasonable also to expect different properties for the magnetoreceptors of mammals, for example, for those involved in learned spatial navigation tasks compared to more innate behaviors like MA or the still enigmatic nest-building preferences (Begall et al., 2013).

3.3. Electromagnetic Induction A moving charged particle always creates a magnetic field. In turn, this implies that a conductor moving through a magnetic field creates an electromotive force that is proportional to the intensity of the magnetic field and the speed and direction of movement with respect to the magnetic field lines ( Jungerman & Rosenblum, 1980). If an animal is moving in a conductive medium like seawater and if it is sensitive enough to detect the minimal voltages that are created by its own movement, it could in theory deduce the compass direction in which it swims because this is encoded in the small differences in the voltages created (Kalmijn, 1984). Elasmobranch fish such as sharks and rays possess electroreception organs, the ampullae of Lorenzini, which are sensitive enough to detect magnetic fields of EMF strength (Kalmijn, 1966, 1971; Murray, 1962; Paulin, 1995). The finding that elasmobranchs can indeed sense magnetic fields (Kalmijn, 1982; Meyer, Holland, & Papastamatiou, 2005) led to the parsimonious assumption that they use their electroreceptors also for this purpose. However, direct conclusive evidence is still missing. Since

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electromagnetic induction as a means of sensing magnetic fields is dependent on the electric circuit between the animal and the surrounding medium, it is highly unlikely that this mechanism is used by nonmarine animals, for which the circuit would have to be enclosed inside the animal in order to work ( Jungerman & Rosenblum, 1980). Even though some mammals such as the platypus Ornithorhynchus anatinus and the Guiana dolphin Sotalia guianensis have been shown to possess structures that are evolutionarily convergent with Lorenzini’s ampullae and enable their hosts to sense electric fields, the sensitivity of these receptors is several magnitudes lower than in elasmobranchs and thus does not reach the theoretical threshold for detection of the geomagnetic field (Czech-Damal et al., 2011; Peters, Eeuwes, & Bretschneider, 2007; Scheich, Langner, Tidemann, Coles, & Guppy, 1986). Therefore, it is highly probable that these mammals use their electroreception organs exclusively for detection of prey. In fact, some experiments have even raised concerns about whether any animal makes use of the induction mechanism of magnetoreception, since rays are affected by magnets attached to their head, which would not interfere with an induction mechanism of magnetoreception since they move in parallel with the animal (Kirschvink et al., 2001).

4. DO WE (HUMANS) SENSE THE MAGNETIC FIELD? In the 1970s and 1980s, Robin Baker performed a series of studies on human magnetic orientation (Baker, 1980, 1989, and references cited therein) with high school and college students mainly recruited from Manchester University. Basically, three different types of experiments were performed: In the simplest version (so-called “walkabouts”), guides led sighted groups of students on winding paths (2–4 km) through unfamiliar dense woodlands and asked them at the respective test sites (approximately 1 km away from “home”) to indicate the “home” direction (i.e., the direction of the starting point), to name the cardinal direction of “home,” and to estimate the straight-line distance to “home.” In the so-called “bus experiments,” Baker transported blindfolded students on indirect routes by buses or vans to release sites 6–52 km from the starting points (Manchester University ¼ “home”). Before and after their release, the students were asked similar questions as in the “walkabouts.” According to statistical analysis, the directions were significantly clustered around the “home” direction with a standard deviation of less than 45
. In the last

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set of tests (chair experiments), blindfolded students wearing earmuffs were rotated on a chair by an experimenter. Each time the experimenter stopped the chair, the subjects were asked to indicate the direction in which they were facing. Again, the results showed that subjects were able to indicate directions better than would be expected if they were relying only on chance. Murphy (working as a PhD candidate under Baker at Manchester University) elaborated on the “chair experiments” and tested approximately 1300 subjects aged between 4 and 20 years. She confirmed Baker’s finding that humans are able to indicate the cardinal directions and found that females between 11 and 18 years performed best (Murphy, 1989). Campion, also being inspired by Baker and his “chair experiments,” asked whether humans could develop a sense of direction when unable to orient successfully at first. She tested eight subjects, each several times, with the aim that the subjects learn to locate north during the course of the study. Only four subjects developed an ability to indicate north and performed better than chance at the end of the study—the other four remained unable to orientate throughout the experiment (Campion, 1991). Baker performed his tests also under altered magnetic fields either by attaching bar magnets to helmets that the students wore during the outward journey in the bus experiments or walkabouts, or by means of Helmholtz coils in the chair experiments (the helmets of the control group were equipped with brass bars of equivalent weight). By contrast, Murphy (1989) used bar magnets that were attached to the subjects’ temples for her “chair experiments.” The three experimental set-ups showed that the control groups performed significantly better than the groups who were tested in artificial magnetic fields. Baker concluded that humans are able to use nonvisual cues to orientate, and possibly also magnetic cues. In the 1980s, different researchers in different countries made several attempts to replicate the “Manchester studies” (mainly “bus and chair experiments”). However, all of them failed and Baker’s methodological approach and statistical analyses have been criticized sharply (Able & Gergits, 1985; Adler & Pelkie, 1985; Fildes, O’Loughlin, Bradshaw, & Ewens, 1984; Gould, 1980, 1985; Gould & Able, 1981; Judge, 1985; Kirschvink, Peterson, Chwe, Filmer, & Roder, 1985; Westby & Partridge, 1986). Baker reanalyzed the results of all studies in which he was not directly involved by employing a statistical procedure that combines probabilities from the V-Test and found a significant deviation from randomness (Baker, 1987). However, this approach has been rebutted since the applied method of statistical meta-analysis was not appropriate (Bovet, 1992) and the vast number

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of negative results speaks against Baker’s methods to prove a human sense of magnetoreception unambiguously. Recently, a researcher has tried again to replicate and extend Baker’s studies (Platt, 2009). Platt stated wrongly that “aside from Baker, no researchers have attempted to replicate this finding” (i.e., the outcome of the “bus experiment”) (p. 29). However, Platt’s “bus experiment,” like previous attempts to replicate Baker’s work, gave no indication that blindfolded and ear-muffed humans could point “homewards.” Curiously, subjects with round magnets attached to their temples did not show a random distribution of directional estimates as in Baker’s study (Baker, 1980) but pointed consistently in the same direction. In a second experiment (similar to Murphy’s “chair experiments”), Platt found that there were no significant differences between males and females or between subjects with brass bars and magnets attached. Only when both parameters (sex and treatment) were taken into account, did an ANOVA indicate significant differences. Unfortunately, however, Platt did not perform a post-hoc test, but instead used multiple t-tests to show that males wearing magnets performed significantly better when asked to indicate cardinal directions than males wearing brass bars. This finding is consistent with the results of his “bus experiments” but is counterintuitive. In a third experiment, Platt tested two males and two females repeatedly over a period of up to 3 months in a discriminant-learning assay. The subjects had to discriminate between presence and absence of a strong static electromagnetic field anomaly with an intensity of approximately 0.67 mT at the centre of the field. While two subjects failed to acquire the ability to detect the magnetic field anomaly, the other two showed a slight increase in hits/false alarm ratios over the course of the study. Maybe it is simply wrong to assume that humans, in general, have a “magnetic sense of direction,” because there might be individual differences in sensitivity. Following this logic, the Hawaiian anthropologist Finney chose a different approach. Instead of performing rigorous scientific experiments, he recounted interviews of human long-distance navigators from Polynesia to find out if magnetoreception might play a role in human long-distance navigation (Finney, 1995). Students of Pacific islanders’ navigation previously thought that these navigators always estimate their course by means of visual cues (celestial or horizon) and dead reckoning, which can be regarded as the standard model. Finney (himself having sailed thousands of nautical miles in a traditional double-hulled sailing canoe) presented some case reports bearing a remarkable resemblance to one another: when the traditional long-distance navigators got into a desperate state at some point on

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their voyage, because they were sailing on the open sea thousands of miles from the next island, could not rely on visual cues (overcast sky or during black night without stars being visible) and had no technical devices to determine the course, they suddenly calmed down and intuitively knew the right course. Finney suggests that magnetoreception is an unconscious directional sense in humans that is usually shut down (due to a hierarchical order of orientation senses) but “that skilled noninstrument navigators may be able to turn to magnetoreception for orientation cues of last resort.” The fact that the navigators take only very short naps of 10–20 min during their journeys has been interpreted in the light of the hypothesis that potential magnetoreceptors are “reset” during sleep. But does the geomagnetic field have an influence on human sleep at all? Ruhenstroth-Bauer, Ru¨ther, and Reinertshofer (1987) tested subjects in different sleeping directions (N–S vs. E–W) and determined several sleeping parameters. Only the mean time the subjects needed to enter the phase of rapid eye movement (REM) showed significant differences between the two conditions: the REM latency time was significantly shorter in subjects sleeping in an E–W direction compared to those sleeping in a N–S direction. However, it is not clear whether potential magnetoreceptors are somehow affected or even reset during sleep. In a second set of experiments, Ruhenstroth-Bauer et al. (1993) investigated human brain electrical activity measured by electroencephalography (EEG) of subjects sitting in N–S and E–W direction, respectively. During the sessions, the subjects were asked to clench their right or left fist after a relaxation period. The overall power of the EEG was significantly decreased during relaxation and fist clenching periods of subjects who sat in E–W direction compared to those sitting in N–S direction. In particular, the frequency of the alpha activity (8–13 Hz) seemed to contribute to this difference. Oscillatory activity in the alpha band has been associated with memory processing and attention (Bas¸ar, Bas¸ar-Erog˘lu, Karakas¸, & Schu¨rmann, 2000). At about the same time, Bell and colleagues also performed EEG measurements and tested the sensitivity of humans to artificially produced magnetic fields, either static, alternating at a frequency of 60 Hz or a combination of both, presented during blocks of trials each consisting of 2-s field presentation followed by a 5-s field-off interval (Bell, Marino, & Chesson, 1992). The artificially produced magnetic fields had an intensity of 78 mT and were thus approximately of the same order of intensity as the geomagnetic field. Most subjects showed an increase in EEG activity in the frequency range 1–18.5 Hz during field exposure compared to

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exposure to a sham field. The strongest responses could be detected at the central and parietal electrodes. The authors conclude that electromagnetic fields can be detected in the central nervous system and that this detection happens unconsciously. In addition, a 15-min exposure to pulsed ELF MF with an intensity of 200 mT affected a subject’s resting EEG measured approximately 7 min after the exposure (Cook, Thomas, & Prato, 2004). It was again the alpha activity that was significantly increased after magnetic field exposure compared to the sham session but, in contrast to the study of Bell et al. (1992), the effect was clearly measured at the occipital electrodes and only marginally at the parietal electrodes. In the meantime, plenty of studies dealing with the influence of different magnetic fields (also ELF-modulated radio frequency fields associated with mobile phones) on physiological parameters in humans have been published, resting and evoked EEGs being only two among a great many. Further parameters under study are, for instance, heart rate, vascular flow, immunoreactivity, melatonin production, standing balance performance, anxiety levels, memory, and many more. The findings as to how magnetic fields influence the biology of humans are reviewed in, for example, Cook, Thomas, and Prato (2002), McKay, Prato, and Thomas (2007), McNamee et al. (2009), and Salunke, Umathe, and Chavan (2013) and are not a subject of this review. It should be pointed out, however, that the literature on biological responses to MF is littered with contradictory results. These contradictions have been related to the wide variety of exposure procedures and study designs (e.g., length of exposure, intensity and frequency of MF), different sensitivity of subjects reacting to magnetic stimuli (Legros & Beuter, 2006), and the unknown time-dependency between stimulus presentation and reaction (Cook et al., 2004), to name just a few. Despite the difficulties that artificially produced magnetic fields impose on studies of magnetosensitivity in humans, and despite the variability of their outcomes, it is still important to know in what way magnetic fields influence human biology because they might be related to serious health effects (e.g., higher risk of childhood leukemia, depression, and suicide; cf. Henshaw, 2002). It is equally important to know the receptors and the transduction mechanism responsible for magnetosensitivity in (at least some) humans. There is some evidence supporting the involvement of a light-dependent radical-pair mechanism. Thoss and colleagues found that the visual sensitivity of humans depends on sinusoidal periodic inversions of the vertical component of the geomagnetic field (Thoss, Bartsch,

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Fritzsche, Tellschaft, & Thoss, 2000). In their experiment, the threshold to detect a flashlight spot was significantly increased in subjects facing in a southern direction, if a fluctuating field inverting the vertical component with a low frequency (110 Hz) was applied to the subject’s head, compared to control subjects (facing south in undisturbed geomagnetic field). If the experimental group faced in a western direction, the fluctuating field did not produce this effect. In a further set of experiments (Thoss & Bartsch, 2003; Thoss, Bartsch, Tellschaft, & Thoss, 2002), the researchers tested the visual thresholds of subjects facing in different directions under artificially produced static magnetic fields. Alignment with field lines (i.e., subjects sitting in a N–S direction) led to significantly lower detection thresholds compared to 20
and 70
shifts. Another argument in favor of the radical-pair mechanism in humans is provided by a study by Foley, Gegear, and Reppert (2011). Fruit flies are magnetosensitive and are thought to use a light-dependent radical-pair mechanism mediated by the flavoprotein cryptochrome of type 1 (Gegear, Casselman, Waddell, & Reppert, 2008). Mutant fruit flies deficient in type 1 cryptochrome are not magnetosensitive and fail in a two-choice test discriminating two arms of a T-maze that differ by presence and absence of a magnetic field. Using a transgenic approach, where the human cryptochrome of type 2 is expressed in the fruit flies, restored magnetosensory ability (Foley et al., 2011). But there is also evidence for biogenic magnetite in humans. More than 20 years ago, Kirschvink and colleagues discovered by means of SQUID (superconducting quantum interference devices) and high-resolution TEM (transmission electron microscopy) that human brain tissues, and especially the meninges (Pia and dura mater: >100 million SD crystals per gram tissue), contain quite large amounts of ferromagnetic material of the magnetite/maghemite family (Kirschvink et al., 1992). These crystals have an average size of 30 nm and are typically clumped in groups of 50–100 particles. Many of them resemble those precipitated by magnetotactic bacteria and fish (Walker et al., 1997). But what is the function of magnetite in the human brain? Since it is very unlikely that the magnetite particles have been taken up by consumption, they are presumably formed by biomineralization (Kirschvink et al., 1992). Of course, it has been speculated that human magnetite might be used for the detection of magnetic fields, but the question is how (Zuddas, Faivre, & Duhamel, 2013). In recent years, Banaclocha and his team have speculated that magnetite could play a role in memory formation by astroglia networks and a transduction of magnetic signals produced within the

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neocortex itself (Banaclocha, Bo´kkon, & Banaclocha, 2010). However, this interesting hypothesis still needs to be confirmed.

5. THE IMPACT OF ANTHROPOGENIC MAGNETIC NOISE ON MAMMALS In terms of signal transduction and sensory ecology, “noise” is anything that reduces the amount of information extracted from a signal by a sensory organ of any modality. Noise can result from varying sensitivity of the receptor of the receiver or varying attenuation of the signal during its transmission through the medium, as well as masking of the signal due to interfering signals (Dusenbery, 1992). Evolution has equipped animals with a variety of mechanisms to deal with these uncertainties and react appropriately to maximize the gain of information. On an evolutionary timescale, however, anthropogenic noise has appeared only very recently. Here, we refer to magnetic noise as magnetic fields that are created by an electric current flowing through conductors, which hinder the animal from sensing the geomagnetic field. Like light pollution, magnetic noise has existed since the invention of electricity less than 200 years ago but has greatly increased during the last few decades and will increase even further due to increasing human population, the accompanying growing energy demands, and the upcoming decentralization of power generation in many countries (Smith Stegen & Seel, 2013). A vast body of literature is devoted to the effects of electromagnetic radiation on organisms and especially on human health (Henshaw, 2002; WHO, 2007). Some of these effects (e.g., direct stimulation of myelinated nerve fibers) can be explained by “nonspecific” interactions between cellular processes and the relatively strong electric and magnetic fields that were applied (e.g., reviewed in Santini, Rainaldi, & Indovina, 2009). Other effects (e.g., disruption of melatonin secretion; e.g. Reiter, 1992), however, are created by field strengths, which are too low to trigger cellular effects directly, for example, via electromagnetic induction (Vanderstraeten & Burda, 2012). It has been proposed that these findings might be expressions of phenomena at the magnetoreceptor level (Phillips & Deutschlander, 1997). The mechanistic implications of this assumption (if true) on the (transduction) mechanism are excellently reviewed in the original work and in several more recent publications (Phillips & Deutschlander, 1997; Vanderstraeten & Burda, 2012; Vanderstraeten & Gillis, 2010; Vanderstraeten, Verschaeve, Burda, Bouland, & de Brouwer, 2012). We refer the reader to these works for

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details, while the remaining part of this section will be devoted to some specific features regarding the biological function of magnetoreception in mammals. The discovery of MA in large mammals (Begall et al., 2008) has initiated a series of studies that together suggest a wide distribution of a magnetic sense among mammals. Native European mammals as diverse as red and roe deer ˇ erveny´ et al., 2011), dogs (Hart, Malkemper (Begall et al., 2008), red foxes (C et al., 2013), and diverse other mammalian taxa (in preparation) apparently perceive the geomagnetic field. Although at present we can only speculate about the biological significance of MA in these mammals, it seems not farfetched to state that the sensory equipment would not have sustained a long history of evolutionary adaptation in such different species without having any function at all. Consequently, whatever that function might be, by disturbing the magnetic sense we directly affect the animals. Oscillating 50 Hz fields created by ordinary power lines disrupt MA of cattle (Burda et al., 2009). Under the assumption that MA is mediated by the same receptor mechanism in all mammals, we can infer that power lines as well as underground cables can exert an effect on a substantial number of European mammals. Up to the present, the red fox is the only species for which we can make an educated guess about the function of MA in its everyday behavior, so it will serve as an example here. In Section 2.5.3 we described the relationship between jumping direction and hunting success ˇ erveny´ et al., 2011). Success is maximized in a NE direcrates in red foxes (C tion and foxes prefer to attack in this direction. If the fox’s magnetic sense was disturbed by oscillating magnetic fields, hunting success might drop dramatically. This is directly comparable to the violating effect of acoustic street noise on the hunting success of the greater mouse-eared bat (Siemers & Schaub, 2011). Even though we might assume that fox magnetoreceptors are equipped with filters that render them unsusceptible to rapid and strong natural fluctuations of the magnetic field (e.g., solar storms), the perception of oscillating magnetic fields in the 50/60 Hz range is explicable by some of the prevailing magnetoreception theories and might impair the fox in aligning with the field lines (Vanderstraeten & Gillis, 2010). Thus, as we gain further insight into the biological significance of magnetoreception also in nonmigratory mammals, we should always be aware that by introducing anthropological noise we might directly exert influence the same way as in other sensory modalities. The ecology of any animal is naturally reflected in its sensory equipment, so any study on the environmental impact of large-scale human building operations (roadbeds and tracks, power lines)

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should in future also consult magnetoreception studies before taking final decisions. We would like to stress that man-made magnetic fields should especially be taken into consideration in future laboratory studies as they might exert influences on the outcome of physiological and behavioral experiments. The fundament of scientific experiments is the use of appropriate controls with only one variable/condition differing between experimental and control group. However, if we are conducting experiments (of whatever kind) on a cell, tissue, or animal and the magnetic conditions in the lab are not sufficiently monitored (which is rarely the case), we might overlook an additional factor—the effect of artificial magnetic fields on our subject. Thus, we get an equation with two variables, which is hard to solve. The new findings that standard laboratory animals such as C57BL/6J and CD-1 mice, of which millions are used worldwide in basic and medical research every year, possess a magnetic sense that is extremely sensitive to disturbance through RF and ELF magnetic fields (Phillips et al., 2013; Prato et al., 2013) highlights the need for research that aims at further characterization of the mammalian magnetic sense and its influence on physiology and role in multisensory integration. Not taking into account all of the senses that an animal possesses will inevitably lead to higher variation in the results of both behavioral and cellular studies (e.g., Portelli, Schomay, & Barnes, 2013).

ACKNOWLEDGMENTS H. B. acknowledges support by the Grant Agency of the Czech Republic (project. nr. 506/11/2121). E. P. M. was funded by a PhD fellowship of the German National Academic Foundation (Studienstiftung des deutschen Volkes). We are grateful to Tim Roper and Sue Healy who invited us to write this review. Their valuable comments and corrections to the language helped to improve the chapter. We thank Michael Painter and Lukas Landler for critically reading and commenting on the chapter.

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