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Shifted magnetic alignment in vertebrates: Evidence for neural lateralization?
Journal of Theoretical Biology 399 (2016) 141–147
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Journal of Theoretical Biology journal homepage: www.elsevier.com/locate/yjtbi
Shifted magnetic alignment in vertebrates: Evidence for neural lateralization? E. Pascal Malkemper a,b, Michael S. Painter c, Lukas Landler c,d,n a
Department of General Zoology, Faculty of Biology, University of Duisburg-Essen, Universitätsstrasse. 2, 45117 Essen, Germany Department of Game Management and Wildlife Biology, Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, Kamýcká 129, 165 21 Prague 6, Czech Republic c Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia, United States of America d Research Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), 1030 Vienna, Austria b
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
Many vertebrate taxa consistently align along the magnetic northsouth axis. Meta-analysis shows a consistent mean clockwise rotation from magnetic north-south. Consistent shift may be due to lateralized magnetic processing in the nervous system.
art ic l e i nf o
a b s t r a c t
Article history: Received 5 January 2016 Received in revised form 13 March 2016 Accepted 28 March 2016 Available online 6 April 2016
A wealth of evidence provides support for magnetic alignment (MA) behavior in a variety of disparate species within the animal kingdom, in which an animal, or a group of animals, show a tendency to align the body axis in a consistent orientation relative to the geomagnetic field lines. Interestingly, among vertebrates, MA typically coincides with the north–south magnetic axis, however, the mean directional preferences of an individual or group of organisms is often rotated clockwise from the north–south axis. We hypothesize that this shift is not a coincidence, and future studies of this subtle, yet consistent phenomenon may help to reveal some properties of the underlying sensory or processing mechanisms, that, to date, are not well understood. Furthermore, characterizing the fine structure exhibited in MA behaviors may provide key insights to the biophysical substrates mediating magnetoreception in vertebrates. Therefore, in order to determine if a consistent shift is exhibited in taxonomically diverse vertebrates, we performed a meta-analysis on published MA datasets from 23 vertebrate species that exhibited an axial north–south preference. This analysis revealed a significant clockwise shift from the north–south magnetic axis. We summarize and discuss possible competing hypotheses regarding the proximate mechanisms underlying the clockwise shifted MA and conclude that the most likely cause of such a shift would be a lateralization in central processing of magnetic information. & 2016 Elsevier Ltd. All rights reserved.
Keywords: Magnetoreception Magnetic alignment Lateralization Geomagnetic field Cortical hemispheres Spatial orientation Central sensory processing
1. Background
n
Corresponding author. E-mail address: [email protected] (L. Landler).
http://dx.doi.org/10.1016/j.jtbi.2016.03.040 0022-5193/& 2016 Elsevier Ltd. All rights reserved.
Many animals use the Earth's magnetic field to orient in their environment (Wiltschko and Wiltschko, 2012). For instance, migrating birds use a magnetic compass during seasonal migrations
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(Wiltschko and Wiltschko, 1972), hatchling sea turtles use navigational markers provided by components of the Earth's magnetic field to guide innate migration along the Atlantic gyre (Lohmann et al., 2012), and newts possess a magnetic compass and a magnetic map which is used during navigation (Phillips et al., 2002a). In addition to the so-called ‘goal oriented’ magnetic behaviors, many animals show spontaneous magnetic responses (Begall et al., 2013), often referred to as ‘magnetic alignment’ (MA). As used in this article, MA describes a spontaneous, non-goal directed magnetic response, such as the tendency of animals to spontaneously align their body axis relative to the Earth's magnetic field. Magnetic alignment was first described over 50 years ago in insects (i.e. in European cockchafer, Melolontha melolontha, (Schneider, 1963)), and today evidence suggests that this behavior is commonplace among animals across diverse taxa (Begall et al., 2013). However, although widespread within the animal kingdom, little is known about the sensory mechanisms and the functional significance of MA behaviors. Insects often exhibit quadrimodal spontaneous orientation, aligning along cardinal or anticardinal magnetic axes, (Becker et al., 1996, 1964; Becker and Speck, 1964; Painter et al., 2013; Vácha et al., 2010), whereas vertebrates show preferences to align their body along the north–south magnetic axis (Begall et al., 2008, 2011; Burda et al., 2009; Hart et al., 2012, 2013a, 2013b; Slaby et al., 2013). The same directional tendencies have been shown in spontaneous directional nest construction of some mammals when tested in visually symmetric circular arenas (Malkemper et al., 2015; Oliveriusová et al., 2014). Even though it is controversial whether nest-building preferences represent a form of magnetic alignment equivalent to the alignment behaviors discussed above [see (Begall et al., 2013)], in the current discussion they are considered spontaneous directional responses to the geomagnetic field, and therefore are included in our definition and analysis. Few studies have attempted to investigate the magnetoreception mechanism underlying MA. While subterranean rodents (mole-rats) seem to use a magnetite-based mechanism (MBM) (Marhold et al., 1997; Thalau et al., 2006), evidence from other vertebrates, including epigeic mammals, points towards the involvement of a radical pair mechanism (RPM) (Landler et al., 2015; Malkemper et al., 2015). The RPM has also been implicated in the magnetic compass response of migratory birds and amphibians (Phillips et al., 2010b; Ritz, 2011). However, strong support for a magnetite-based mechanism mediating spontaneous nest building responses comes from mole-rats, the best studied group of mammals for magnetoreception to date. It is, however, unclear whether this represents the general mechanism underlying all vertebrate magnetoreception, or rather, if mole-rats represent the exception to the rule given their unique subterranean lifestyle. Birds and newts seem to possess both types of receptors used for different tasks (Phillips, 1986; Wiltschko et al., 2007). While the underlying mechanisms of MA are poorly understood, even less evidence exists concerning its possible function and biological significance (Begall et al., 2013). The only study linking MA behavior to a biological fitness advantage showed that red foxes were approximately 60 70% more successful at catching hidden prey when mousing jumps were directed towards northeast or south-west, compared to mousing attempts in other magnetic directions (Červený et al., 2011). This observation fits quite well with the idea that animals use a visual pattern that receives input from the geomagnetic field to encode their environment (Phillips et al., 2010a). A biophysical mechanism that creates such a visual pattern has been suggested to underlie magnetic compass responses in a variety of vertebrates (Cintolesi et al., 2003; Ritz et al., 2000), and has been proposed to be generated through a radical pair mechanism (RPM) occurring in specialized photoreceptors of the retina or pineal organ (Hart et al.,
2013a, 2013b; Nießner et al., 2011; Phillips et al., 2010a, 2001). Behavioral evidence from turtles suggests that the same RPM pattern might be involved in encoding novel environments, where an association is formed between novel places and a particular ‘visual’ pattern (Landler et al., 2015). In the case of mousing red foxes, the visual pattern generated from an RPM might act as a range finder helping to estimate prey distances and/or guide the trajectory of the jump (Červený et al., 2011) in a similar way as the patterns has been proposed to facilitate the tendency of waterfowl landing along the north–south magnetic axis (Hart et al., 2013a, 2013b). Interestingly, in cases where animals align axially along the north–south axis, as is the case in most vertebrates, but also reported in some invertebrates (Sandoval et al., 2012), there tends to be a conspicuous shift of the mean alignment clockwise from the magnetic north–south axis. A consistent shift across multiple species during various behaviors (e.g. grazing, sleeping, landing, hunting, nest building) would not be predicted from the hypotheses for the biological function or the underlying receptor mechanism of MA that have been proposed to date. However, such a phenomenon in spatial behaviors might indicate a functional lateralization of the underlying magnetic sensory pathway in vertebrates, as has been suggested in different species of migratory birds but remains a highly debated topic in magnetoreception. While research in different bird species provided evidence for a lateralized magnetic compass located in the right eye (Wiltschko et al., 2002), later evidence challenged these results, possibly suggesting a more complex story involving developmental effects on the underlying sensory mechanism (Gehring et al., 2012; Hein et al., 2011). It is further likely, that there exists a functional lateralization rather than an absolutely lateralized receptor distribution with regard to the magnetic sense, as was deduced from experiments with birds showing ocular dominance, predominantly using one eye over the other depending on the type of magnetic tasks (Wilzeck et al., 2010). Such a functional lateralization might be related to the widespread lateralized central processing of information in vertebrate brains (Halpern et al., 2005; Walker, 1980). Current knowledge about central processing of magnetic information in the brain of vertebrates is limited and mostly based on studies of immediate early gene expression induced by magnetic stimulation (see discussion for details). Based on the findings in birds, two pathways processing magnetic information have been suggested, one for each receptor type (MBM and RPM) (Mouritsen et al., 2015). The pathway for magnetic compass information (mediated by RPM) in the bird brain connects the primary receptors that are believed to reside in the retina via the dorsal lateral geniculate nucleus of the thalamus to the forebrain Cluster N and adjacent hyperpallial areas (Mouritsen et al., 2015). Magnetic map information (mediated by MBM) on the other hand is suggested to be routed via trigeminal brainstem nuclei to the forebrain nucleus basalis and trigeminal parts of the nidopallium (Mouritsen et al., 2015). If these two pathways mediating magnetic information were anatomically and/or functionally lateralized, it would be conceivable that the lateralization results in shifted MA behavior, which could in turn shed light on the enigmatic biological function of vertebrate MA. Here, we performed a meta-analysis of published data after a systematic literature search on vertebrate axial MA responses addressing two main questions: (1) Do mean responses from vertebrate species show a consistent and significant clockwise shift, deviating from the magnetic north–south axis, and (2) what are possible explanations for such a shift in light of evidence on the underlying mechanism and possible adaptive functions?
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2. Method 2.1. Data collection We collected axial MA data of 23 vertebrate species that have been published or have been submitted to a peer-reviewed journal. All species for which data were available are listed in Table 1. Our criteria for inclusion of data were the following: axial response of vertebrate species (excluding unimodal and quadrimodal responses) under natural (full spectrum) light conditions and the data is presented with unweighted data points. We classified distributions according to the difference of their mean vector from pointing towards magnetic north, i.e. 0°, as being either clockwise shifted (1–45°), or counterclockwise shifted (315–0°). Zero degree (0°) was categorized as counterclockwise in order to avoid any bias in favor of our hypothesis. Data from trained assays were excluded from the analysis although, in some cases, spontaneous responses emerged (Muheim et al., 2006). 2.2. Analysis We used the non-parametric exact binominal test (two-tailed) to analyze if the proportion of alignment responses between clockwise and counterclockwise was different from the 0.5 level of chance that would be expected if the animals show no consistent departure from the north–south axis. Furthermore, we combined all available data on axial vertebrate alignment and calculated the mean alignment across studies using Rayleigh test. We calculated the 95% confidence interval in order to test if magnetic north was included in the mean direction. The statistical software R (R Development Core Team, 2012) was used for linear statistics and Oriana 4.02 was used for circular statistics (Kovach, 2011).
3. Results Our literature survey, including data submitted for publication, revealed data sets for axial vertebrate alignment from 10 studies including 23 different species (Table 1). The proportion of CW alignment responses was 0.78, and the exact binominal test
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showed that the proportion of CW to CCW studies was significantly different from the 0.5 chance level (p ¼0.01), suggesting a significant clockwise shift in axial alignment responses. All literature accounts combined showed a highly significant axial alignment towards 9.1°/189.1° (Rayleigh test p o0.0001, r ¼0.931), and the 95% confidence interval did not include magnetic north (4.6–13.5°/184.6–193.5°; see Fig. 1).
4. Discussion The presented data provide evidence for a consistent shift in vertebrate magnetic alignment behavior that deviates significantly clockwise from magnetic north. Not only is it intriguing that such a diverse range of species show axially symmetrical spatial behavior aligned spontaneously along the north–south magnetic axis, but also that a consistent clockwise shift seems to be ubiquitous across vertebrates exhibiting axial MA behavior, and could be interpreted as evidence for similarity of the underlying sensory mechanism and/or its adaptive functionality. The deviation from the magnetic north–south axis could originate at different levels in the sensory hierarchy: (1) it could be related to asymmetries at the receptor level, or (2) to functional brain asymmetries, i.e. central processing. We will discuss both possibilities below. 4.1. Asymmetries at the receptor level Although the exact nature of animal magnetoreceptors is still unknown, the results of several behavioral experiments with migratory birds suggest that magnetic compass responses are mediated by the eyes, and there is evidence that this processes may be lateralized, located in the right eye (Gehring et al., 2012; Wiltschko et al., 2003; Wiltschko et al., 2002). This lateralization of magnetic compass responses, which is thought to be mediated by a ‘light-dependent’ magnetoreceptor, was, however, heavily discussed and claimed not to be a common feature in birds (Hein et al., 2011, 2009). It is unclear if lateralization at the receptor level is a general feature across all vertebrates, but if so, it could contribute to lateralized magnetic behaviors, such as the shift in MA presented here. Animals may tend to center, or align such a
Table 1 Collection of literature data included in the study. Only data sets with statistically significant axial mean directions (Rayleigh test) were included. We defined only mean axial directions (Mean dir.) between 1° and 45° as being clockwise-shifted ('CW-shift'). Author
Year
Phillips et al. (2002b) Hart et al. (2012a, 2013b) Begall et al. (2008) Begall et al. (2008) Begall et al. (2008) Červený et al. (2016) Červený et al. (2016) Oliveriusová et al. (2014) Malkemper et al. (2015) Kušta et al. (in preparation) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b)
Class
Order
Species
Location
Mean dir. (deg)
CW-shift
Amphibia Teleostei Mammalia
Caudata Cypriniformes Artiodactyla
Notophthalmus viridescens Cyprinus carpio Cervus elaphus Capreolus capreolus Bos primigenius Sus scrofa Phacochoerus africanus Clethrionomys glareolus Apodemus sylvaticus Lepus europaeus Alopochen aegyptiacus Anas penelope Anas platyrhynchos Aythya ferina Cygnus olor Dendrocygna viduata Larus canus Larus ridibundus Mergellus albellus Mergus merganser Nettapus auritus Vanellus armatus Vanellus coronatus
USA Czech Republic Global Global Global Czech Republic South Africa Czech Republic Czech Republic Czech Republic Botswana Finland Europe, North-America Poland Europe Botswana Finland Europe Finland Finland Botswana Botswana Botswana
38 8 10 9 6 17 25 0 23 15 175 7 9 8 3 4 6 19 3 5 176 177 179
Yes Yes Yes Yes Yes Yes Yes No Yes Yes No Yes Yes Yes Yes Yes Yes Yes Yes Yes No No No
Rodentia
Aves
Lagomorpha Anseriformes
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Fig. 1. Mean axial orientations of 23 different vertebrate species. The two-headed arrow represents the mean vector (mean direction: 9°/189°); the arrow length is proportional to the mean vector length (r ¼0.931), with the radius of the circle equal to 1 (i.e. r ¼ 1). Each pair of opposite symbols represents the mean axial orientation of one alignment study. The dotted circle represents the threshold for a mean vector length that would result in p ¼ 0.001. Dotted lines represent the 95% confidence interval around the mean (4.6–13.5°/184.6–193.5°). Data are plotted relative to magnetic north.
lateralized receptor system (e.g. right or left eye) with the north– south axis/field lines (i.e. most salient reference point) resulting in a slightly shifted body axis of the individual relative to the magnetic field lines (all species included in the analysis have laterally positioned eyes). From physical models it can be adduced that the visual pattern produced by the hypothesized RPM could be realized as an axially symmetrical pattern at the sensory level, e.g. visual system (Ritz et al., 2000; Solov'yov et al., 2010). In the proposed models, the north–south axis of the geomagnetic field constitutes the major axis of this pattern. If central parts of that pattern (i.e. the strongest/weakest signal of the pattern) provide a more salient spatial cue for navigation or MA behaviors (Begall et al., 2013; Phillips et al., 2010a), aligning lateralized receptors would result in a slightly shifted alignment of the axis of the organism with respect to the magnetic field lines. Interestingly, the photoreceptor distribution in some birds shows slight differences between the left and the right eye (Hart, 2001). The left eye possesses more single cones which are important for spectral discrimination and high visual acuity, while the right eye possesses more double-cones which are essential for the detection of motion. Although the differences are small, they are associated with a clear behavioral lateralization (Güntürkün et al., 2000), and therefore provide the possibility that a similar lateralization may underlie MA behaviors. Cryptochromes, blue-light sensitive flavoproteins, have been proposed as the putative magnetoreceptor molecules mediating a RPM in invertebrates and vertebrates, because their spectral and chemical properties fit with most behavioral and histological evidence (Dodson et al., 2013). In birds, one type of cryptochrome, cryptochrome 1a, is present in the outer segments of all cones that contain opsins sensitive to light in the ultraviolet spectrum (UV cones). This is consistent with theoretical proposals for an involvement of cryptochrome 1a in creating a magnetic visual pattern (Nießner et al., 2011). Interestingly, these cryptochromecontaining UV cones have been shown to be up to 20% more abundant in the left eye of the European starling than in the right eye (Hart et al., 2000a). This might indicate that also cryptochrome 1a is asymmetrically distributed. The only additional quantitative study on bilateral photoreceptor distribution was done on blue tits and blackbirds, where UV cones were not found in significantly
higher densities in the left eye (Hart et al., 2000b). However, it has been argued that several mammal species, despite showing clear MA (e.g. ungulates), do not express cryptochrome 1 in their blue cones (homologous to avian UV cones, Nießner et al. (2016)) Therefore, with the exception of European starlings, the data available does not support an asymmetric cryptochrome distribution providing the basis for the MA-shift. Clearly, future histological studies of cryptochrome's distribution across species in different seasonal, physiological and developmental states will provide additional support for, or against, the role of lateralization underlying MA behavior. Finally, newts, which also show a clockwise shifted MA, appear to have their light dependent magnetoreceptor in the parietal eye, a homolog to the pineal organ of other vertebrates, rather than the retina (Deutschlander et al., 1999). This organ is unpaired, and consequently has no conceivable lateralization. Therefore, if the consistent shift in MA results from a common factor across all species, a functional lateralization at the RPM receptor-level is unlikely to be the cause. Another idea that can be related to receptor lateralization was proposed by Phillips et al. (2002b) and assumes a magnetite-based magnetoreceptor (MBM) underlying MA, or a combination of MBM and the previously mentioned RPM. Magnetite-based magnetoreception is an alternative mechanism to the RPM, where magnetite particles are thought to provide the animals with a magnetometer and/or magnetic compass (Kirschvink et al., 2001). For most epigeic vertebrates studied so far it is assumed that they possess both magnetoreceptors (RPM and MBM), with the RPM providing a magnetic compass and the MBM providing magnetic ‘map’ information (magnetic latitudinal or longitudinal position may be derived using spatial gradients, e.g. intensity and/or inclination, provided by the magnetic field) (Phillips, 1986; Wiltschko and Wiltschko, 2007). In order to perceive a consistent and comparable 'map reading', the animals would reduce variation in the magnetic measurements by rotating the receptor towards a consistent alignment, likely using the magnetic field lines to guide this alignment behavior. They might achieve this by using the RPM compass to align the map receptor with respect to the field lines and then take the reading (Phillips et al., 2002b). A lateralized magnetite based map detector could theoretically cause a corresponding shift of the alignment axis. In fact, measurements of the natural remanent magnetism (NRM) of 18 newts showed individual differences in the NRM declination (in relation to the newts' body axis). Furthermore, when tested under full spectrum light, the NRM declinations seemed to correlate with the newts' alignment responses (Phillips et al., 2002b). However, it is unclear if the NRM declination is related to a magnetite receptor at this stage of the research. Phillips et al. (2002b) also proposed that the alignment they found under long-wavelength, where the RPM system is not expected to function, is based on a ‘systematic sampling strategy’ to find the alignment of the ‘map receptor’ and therefore the reliable map reading. It is worth noting that also under such long-wavelength conditions, which are not included in this current meta-analysis, the alignment was shifted clockwise. Further studies would be needed to determine if magnetite is generally involved in MA and if there is a general directional bias in magnetite receptors. In addition, because of recent failures to locate a MBM (Edelman et al., 2015; Treiber et al., 2012), such questions might remain unexplored until a vertebrate MBM is confirmed by histological studies. 4.2. Asymmetries at the level of the central nervous system It is well established that many animals show lateralized control of a great variety of different behaviors (reviewed in Duboc et al., 2015; Rogers and Andrew, 2002). Such lateralization can differ between individuals (individual bias) or be consistent within
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a whole population (population wide bias). Only a population wide bias that extends across species could explain the consistent shift in MA. Behavioral lateralization is based on specialization of the cortical hemispheres or unilateral nerve centers to accomplish certain tasks, which are then not directly fulfilled by the contralateral equivalent. Consequently, behaviors become lateralized as many motor systems and many sensory organs are unilaterally innervated. Below we will give some examples and discuss how they could explain the MA shift. In many vertebrates, dominance of one hemisphere during certain behaviors is expressed in a predominant use of a single eye during a particular task. The left eye has been shown to be especially important during the visual assessment of space, especially for the use of distant visual features for orientation and the detection of threats (Duboc et al., 2015; Rogers and Andrew, 2002). Such visuospatial right-hemispheric dominance seems to be a general vertebrate trait as it has been well documented in birds (McKenzie et al., 1998; Rashid and Andrew, 1989), cattle (Robins and Phillips, 2010), rodents (Cowell et al., 1997), and primates including humans (Hopkins and Morris, 1989; Wendt and Risberg, 1994). It has been argued that the cryptochrome-based magnetic field perception (mediated by a RPM) serves as a visual grid that helps to put landmarks into global perspective (Phillips et al., 2010a). It is reasonable to assume that the central axis of this symmetrical pattern would be predominantly perceived via the eye that is specialized on spatial tasks; the left eye in vertebrates (see above). Correspondingly, in magnetic conditioning experiments it has been demonstrated that pigeons use the right eye for goal-directed determination of magnetic compass directions while usage of the left eye led to axial responses (Wilzeck et al., 2010). The left eye seems to be preferred during non-goal directed tasks, such as spontaneous magnetic alignment and would help to explain the clockwise shift, if the left eye was aligned with magnetic north. Thus, it is conceivable that the clockwise shift observed in MA studies is based on a lateralized higher processing of magnetic information. Unfortunately, the neuronal processes underlying magnetic orientation are still unclear. A number of studies in bird and rodent species have shown activation of certain brain regions in response to magnetic stimuli; usually immediate early genes are used as correlates for neuronal activation (i.e. ZENK (Heyers et al., 2007, 2010; Lefeldt et al., 2014; Liedvogel et al., 2007; Mouritsen et al., 2005; Shimizu et al., 2004) and c-fos (Burger et al., 2010; Němec et al., 2001; Wu and Dickman, 2011)). Electrophysiological methods have also revealed neuronal responses to magnetic field changes (Semm and Demaine, 1986; Semm and Beason, 1990; Semm et al., 1984; Vargas et al., 2006; Wu and Dickman, 2012, but see Ramírez et al., 2014). In birds, brain regions involved in magnetoreception seem to be brainstem nuclei of the trigeminal and vestibular system as well as the hippocampus (Lefeldt et al., 2014; Semm et al., 1984; Wu and Dickman, 2011). Furthermore, a specific region of the bird forebrain (Cluster N) is crucial for magnetic orientation in night migrants, although its functional role within the system is unknown (Mouritsen et al., 2005; Zapka et al., 2009). In mammals, magnetic activation has been detected in the hippocampus, the superior colliculus and the primary somatosensory cortex (Burger et al., 2010; Němec et al., 2001). In many studies, neuronal activation in response to magnetic fields has been found bilaterally without evidence of lateralization (reviewed in Mouritsen and Hore, 2012). This does, however, not dissent with the idea of a task-dependent lateralization of magnetic behaviors as it is suggested by the findings of Wilzeck et al. (2010). For example, none of the neuronal activations studies used magnetic alignment to induce neuronal activity. Furthermore, when it was specifically
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addressed, a significant left eye/right hemisphere dominance was demonstrated within Cluster N during a magnetic orientation task in European robins and two warbler species (Liedvogel et al., 2007). Further detailed investigations of lateralization in all parts of the central pathway of magnetic information during different magnetic tasks is clearly needed (see Wilzeck et al., 2010). Finally, lateralized processing of magnetic information does not necessarily lead to lateralized activation of primary magnetoreceptive areas, but might be confined to higher order association areas. 4.3. Conclusion Following an a priori established criteria, our meta-analysis shows a highly significant magnetic alignment across vertebrate species along the north–south axis. However, a consistent clockwise shift from the exact north–south axis is an evident and intriguing feature of this behavior and is consistent across multiple vertebrate species. One could argue that such a consistent bias could provide insights into the underlying physiological mechanism of magnetoreception. We theorized that a bias could, in principle, originate at two different, but not necessarily exclusive, levels: asymmetries at the receptor level, or of central processing. Evidence for or against lateralization of the magnetoreceptors is currently weak and progress is hampered by the fact that the magnetoreceptors are still unknown. For the most probable candidate, cryptochrome 1, weak evidence for lateralization exists, but without further and stronger evidence it is difficult to argue that a cryptochrome asymmetry is responsible for the MA shift. On the other hand, behavioral lateralization has been conclusively and consistently shown among several vertebrate orders and the proposed functional asymmetry between the left and right eye is in line with a hypothetical spatial function of RPM-based magnetoreceptors. Thus, we conclude that a general lateralization of the central nervous system, which has been found to be a common vertebrate trait, is the most probable origin of the MA-shift. However, the presented paper should be seen as a thoughtprovoking and hypothesis-generating analysis, hopefully encouraging new research leading to a deeper understanding of spontaneous magnetic preferences in animals. Therefore, we conclude this paper by posing three essential questions that should be addressed in future research on vertebrate magnetic alignment: 1. What is the magnetoreception mechanism underlying magnetic alignment (RPM and/or MBM)? 2. Is the MA-shift lost or reverted when the left eye is covered? 3. What is the adaptive significance of MA, e.g. is it involved in the calibration/reading of a magnetic map and/or does it have a role in magnetic navigation?
Acknowledgments This research was supported by the Grant Agency of the Czech Republic (Project no. 15-21840S to EPM). We thank Sabine Begall, Hynek Burda, Sara-Maria Schnedl and three anonymous reviewers for valuable comments on earlier versions of the manuscript.
References Becker, E., Hemmersbach, R., Stockem, W., 1996. Einfluss niederfrequenter Magnetfelder auf das Orientierungsverhalten von Einzellern: Neue Erkenntnisse zur biologischen Wirkung elektromagnetischer Wechselfelder. DLR Nachrichten
146
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81, 22–26. Becker, G., 1964. Reaktion von Insekten auf Magnetfelder, elektrische Felder und atmospherics. Z. für Angew. Èntomol. 54, 75–88. Becker, G., Speck, U., 1964. Untersuchungen über die Magnetfeld-Orientierung von Dipteren. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 49, 301–340. Begall, S., Červený, J., Neef, J., Vojtěch, O., Burda, H., 2008. Magnetic alignment in grazing and resting cattle and deer. Proc. Natl. Acad. Sci. 105, 13451–13455. Begall, S., Malkemper, E.P., Červený, J., Němec, P., Burda, H., 2013. Magnetic alignment in mammals and other animals. Mamm. Biol. 78, 10–20. Begall, S., Burda, H., Červený, J., Gerter, O., Neef-Weisse, J., Němec, P., 2011. Further support for the alignment of cattle along magnetic field lines: reply to Hert et al. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol., 1–7. Burda, H., Begall, S., Červený, J., Neef, J., Němec, P., 2009. Extremely low-frequency electromagnetic fields disrupt magnetic alignment of ruminants. Proc. Natl. Acad. Sci. 106, 5708–5713. Burger, T., Lucová, M., Moritz, R.E., Oelschläger, H.H.A., Druga, R., Burda, H., Wiltschko, W., Wiltschko, R., Němec, P., 2010. Changing and shielded magnetic fields suppress c-Fos expression in the navigation circuit: input from the magnetosensory system contributes to the internal representation of space in a subterranean rodent. J. R. Soc. Interface 7, 1275–1292. Červený, J., Begall, S., Koubek, P., Nováková, P., Burda, H., 2011. Directional preference may enhance hunting accuracy in foraging foxes. Biol. Lett. 7, 355–357. Červený J., Burda H., Ježek M., Kušta T., Husinec V., Nováková P., Hart V., Hartová V., Begall S. and Malkemper E.P., 2016. Magnetic alignment in wild boars (Sus scrofa) and warthogs (Phacochoerus africanus). Mammal Review, in press. Cintolesi, F., Ritz, T., Kay, C.W.M., Timmel, C.R., Hore, P.J., 2003. Anisotropic recombination of an immobilized photoinduced radical pair in a 50-[mu] T magnetic field: a model avian photomagnetoreceptor. Chem. Phys. 294, 385–399. Cowell, P., Waters, N., Denenberg, V., 1997. The effects of early environment on the development of functional laterality in Morris maze performance. Laterality: asymmetries of body. Brain Cogn. 2, 221–232. Deutschlander, M.E., Borland, S.C., Phillips, J.B., 1999. Extraocular magnetic compass in newts. Nature 400, 324–325. Dodson, C.A., Hore, P.J., Wallace, M.I., 2013. A radical sense of direction: signalling and mechanism in cryptochrome magnetoreception. Trends Biochem. Sci. 38, 435–446. Duboc, V., Dufourcq, P., Blader, P., Roussigné, M., 2015. Asymmetry of the brain: development and implications. Annu. Rev. Genet. 49, 647–672. Edelman, N.B., Fritz, T., Nimpf, S., Pichler, P., Lauwers, M., Hickman, R.W., PapadakiAnastasopoulou, A., Ushakova, L., Heuser, T., Resch, G.P., Saundersd, M., Shawd, J.A., Keays, D.A., 2015. No evidence for intracellular magnetite in putative vertebrate magnetoreceptors identified by magnetic screening. Proc. Natl. Acad. Sci. 112, 262–267. Gehring, D., Wiltschko, W., Güntürkün, O., Denzau, S., Wiltschko, R., 2012. Development of lateralization of the magnetic compass in a migratory bird. Proc. R. Soc. B: Biol. Sci. 282, 1–6. Güntürkün, O., Diekamp, B., Manns, M., Nottelmann, F., Prior, H., Schwarz, A., Skiba, M., 2000. Asymmetry pays: visual lateralization improves discrimination success in pigeons. Curr. Biol. 10, 1079–1081. Halpern, M.E., Güntürkün, O., Hopkins, W.D., Rogers, L.J., 2005. Lateralization of the vertebrate brain: taking the side of model systems. J. Neurosci. 25, 10351–10357. Hart, N., Partridge, J., Cuthill, I., 2000a. Retinal asymmetry in birds. Curr. Biol. 10, 115–117. Hart, N., Partridge, J., Cuthill, I., Bennett, A.T., 2000b. Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.). J. Comp. Physiol. A 186, 375–387. Hart, N.S., 2001. The visual ecology of avian photoreceptors. Progress Retin. Eye Res. 20, 675–703. Hart, V., Malkemper, E.P., Kušta, T., Begall, S., Nováková, P., Hanzal, V., Pleskač, L., Ježek, M., Policht, R., Husinec, V., 2013a. Directional compass preference for landing in water birds. Front. Zool. 10, 38. Hart, V., Novakova, P., Malkemper, E.P., Begall, S., Hanzal, V., Jezek, M., Kusta, T., Nemcova, V., Adamkova, J., Benediktova, K., Červený, J., Burda, H., 2013b. Dogs are sensitive to small variations of the Earth's magnetic field. Front. Zool. 10, 80. Hart, V., Kusta, T., Nemec, P., Blahova, V., Jezek, M., Novakova, P., Begall, S., Cerveny, J., Hanzal, V., Malkemper, E.P., Stipek, K., Vole, C., Burda, H., 2012. Magnetic alignment in carps: evidence from the Czech christmas fish market. PLoS One 7, e51100. Hein, C.M., Engels, S., Kishkinev, D., Mouritsen, H., 2011. Robins have a magnetic compass in both eyes. Nature 471, E1. Hein, C.M., Zapka, M., Heyers, D., Kutzschbauch, S., Schneider, N.-L., Mouritsen, H., 2009. Night-migratory garden warblers can orient with their magnetic compass using the left, the right or both eyes. J. R. Soc. Interface, 20090376. Heyers, D., Manns, M., Luksch, H., Güntürkün, O., Mouritsen, H., 2007. A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLoS One 9, e937. Heyers, D., Zapka, M., Hoffmeister, M., Wild, J., Mouritsen, H., 2010. Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. Proc. Natl. Acad. Sci. USA 107, 9394–9399. Hopkins, W.D., Morris, R.D., 1989. Laterality for visual-spatial processing in two language-trained chimpanzees (Pan troglodytes). Behav. Neurosci. 103, 227. Kirschvink, J.L., Walker, M.M., Diebel, C.E., 2001. Magnetite-based
magnetoreception. Curr. Opin. Neurobiol. 11, 462–467. Kovach, W.L., 2011. Oriana – Circular Statistics for Windows Ver. 4. Kovach Computing Services, Pentraeth, Wales, UK. Kušta T., Červený J., Ježek M., Koubek P., Begall S., Malkemper E.P. and Burda H., Magnetic alignment in European hares (Lepus europaeus). In preparation. Landler, L., Painter, M.S., Youmans, P.W., Hopkins, W.A., Phillips, J.B., 2015. Spontaneous magnetic alignment by yearling snapping turtles: rapid association of radio frequency dependent pattern of magnetic input with novel surroundings. PLoS One 10, e0124728. Lefeldt, N., Heyers, D., Schneider, N.-L., Engels, S., Elbers, D., Mouritsen, H., 2014. Magnetic field-driven induction of ZENK in the trigeminal system of pigeons (Columba livia). J. R. Soc. Interface 11. Liedvogel, M., Feenders, G., Wada, K., Troje, N.F., Jarvis, E.D., Mouritsen, H., 2007. Lateralized activation of cluster N in the brains of migratory songbirds. Eur. J. Neurosci. 25, 1166–1173. Lohmann, K.J., Putman, N.F., Lohmann, C.M.F., 2012. The magnetic map of hatchling loggerhead sea turtles. Curr. Opin. Neurobiol. 22, 336–342. Malkemper, E.P., Eder, S.H.K., Begall, S., Phillips, J.B., Winklhofer, M., Hart, V., Burda, H., 2015. Magnetoreception in the wood mouse (Apodemus sylvaticus): influence of weak frequency-modulated radio frequency fields. Sci. Rep., 4. Marhold, S., Wiltschko, W., Burda, H., 1997. A magnetic polarity compass for direction finding in a subterranean mammal. Naturwissenschaften 84, 421–423. McKenzie, R., Andrew, R.J., Jones, R.B., 1998. Lateralisation in chicks and hens: new evidence for control of response by the right eye system. Neuropsychologia 36, 51–58. Mouritsen, H., Hore, P.J., 2012. The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds. Curr. Opin. Neurobiol. 22, 343–352. Mouritsen, H., Heyers, D., Güntürkün, O., 2015. The neural basis of long-distance navigation in birds. Annu. Rev. Physiol. Mouritsen, H., Feenders, G., Liedvogel, M., Wada, K., Jarvis, E.D., 2005. Night-vision brain area in migratory songbirds. Proc. Natl. Acad. Sci. USA 102, 8339–8344. Muheim, R., Edgar, N.M., Sloan, K.A., Phillips, J.B., 2006. Magnetic compass orientation in C57BL/6J mice. Learn. Behav. 34, 366–373. Němec, P., Altmann, J., Marhold, S., Burda, H., Oelschläger, H.H., 2001. Neuroanatomy of magnetoreception: the superior colliculus involved in magnetic orientation in a mammal. Science 294, 366–368. Nießner, C., Denzau, S., Malkemper, E.P., Gross, J.C., Burda, H., Winklhofer, M., Peichl, L., 2016. Cryptochrome 1 in retinal cone photoreceptors suggests a novel functional role in mammals. Sci. Rep. 6, 21848. Nießner, C., Denzau, S., Gross, J.C., Peichl, L., Bischof, H.-J., Fleissner, G., Wiltschko, W., Wiltschko, R., 2011. Avian ultraviolet/violet cones identified as probable magnetoreceptors. PLoS One 6, e20091. Oliveriusová, L., Němec, P., Pavelková, Z., Sedláček, F., 2014. Spontaneous expression of magnetic compass orientation in an epigeic rodent: the bank vole, Clethrionomys glareolus. Naturwissenschaften 101, 557–563. Painter, M.S., Dommer, D.H., Altizer, W.W., Muheim, R., Phillips, J.B., 2013. Spontaneous magnetic orientation in larval Drosophila shares properties with learned magnetic compass responses in adult flies and mice. J. Exp. Biol. 216, 1307–1316. Phillips, J.B., 1986. Two magnetoreception pathways in a migratory salamander. Science 233, 765–767. Phillips, J.B., Muheim, R., Jorge, P.E., 2010a. A behavioral perspective on the biophysics of the light-dependent magnetic compass: a link between directional and spatial perception? J. Exp. Biol. 213, 3247–3255. Phillips, J.B., Jorge, P.E., Muheim, R., 2010b. Light-dependent magnetic compass orientation in amphibians and insects: candidate receptors and candidate molecular mechanisms. J. R. Soc. Interface 7 (Suppl. 2), S241–S256. Phillips, J.B., Deutschlander, M.E., Freake, M.J., Borland, S.C., 2001. The role of extraocular photoreceptors in newt magnetic compass orientation: parallels between light-dependent magnetoreception and polarized light detection in vertebrates. J. Exp. Biol. 204, 2543–2552. Phillips, J.B., Freake, M.J., Fischer, J.H., Borland, C., 2002a. Behavioral titration of a magnetic map coordinate. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 188, 157–160. Phillips, J.B., Borland, S.C., Freake, M.J., Brassart, J., Kirschvink, J.L., 2002b. ‘Fixedaxis’ magnetic orientation by an amphibian: non-shoreward-directed compass orientation, misdirected homing or positioning a magnetite-based map detector in a consistent alignment relative to the magnetic field? J. Exp. Biol. 205, 3903–3914. R Development Core Team, 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Ramírez, E., Marín, G., Mpodozis, J., Letelier, J.-C., 2014. Extracellular recordings reveal absence of magneto sensitive units in the avian optic tectum. J. Comp. Physiol. A 200, 983–996. Rashid, N., Andrew, R.J., 1989. Right hemisphere advantages for topographical orientation in the domestic chick. Neuropsychologia 27, 937–948. Ritz, T., 2011. Quantum effects in biology: bird navigation. Proc. Chem. 3, 262–275. Ritz, T., Adem, S., Schulten, K., 2000. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707–718. Robins, A., Phillips, C., 2010. Lateralised visual processing in domestic cattle herds responding to novel and familiar stimuli. Laterality 15, 514–534. Rogers, L.J., Andrew, R., 2002. Comparative Vertebrate Lateralization. Cambridge University Press. Sandoval, E.L., Wajnberg, E., Esquivel, D.M., de Barros, H.L., Acosta-Avalos, D., 2012. Magnetic Orientation in Solenopsis sp. ants. J. Insect Behav. 25, 612–619. Schneider, F., 1963. Systematische Variationen in der elektrischen, magnetischen,
E.P. Malkemper et al. / Journal of Theoretical Biology 399 (2016) 141–147
und geographisch-ultraoptischen Orientierung des Maikafers. Vierteljahrsschr. der Naturforschenden Ges. Zur. 108, 373–416. Semm, P., Demaine, C., 1986. Neurophysiological properties of magnetic cells in the pigeon's visual system. J. Comp. Physiol. A: Neuroethol. Sens., Neural Behav. Physiol. 159, 619–625. Semm, P., Beason, R., 1990. Responses to small magnetic variations by the trigeminal system of the Bobolink. Brain Res. Bull. 25, 735–740. Semm, P., Nohr, D., Demaine, C., Wiltschko, W., 1984. Neural basis of the magnetic compass: interactions of visual, magnetic and vestibular inputs in the pigeon's brain. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 155, 283–288. Shimizu, T., Bowers, A.N., Budzynski, C.A., Kahn, M.C., Bingman, V.P., 2004. What does a pigeon (Columba livia) brain look like during homing? Selective examination of ZENK expression. Behav. Neurosci. 118, 845. Slaby, P., Tomanova, K., Vácha, M., 2013. Cattle on pastures do align along the North–South axis, but the alignment depends on herd density. J. Comp. Physiol. A, 1–7. Solov'yov, I.A., Mouritsen, H., Schulten, K., 2010. Acuity of a cryptochrome and vision-based magnetoreception system in birds. Biophys. J. 99, 40–49. Thalau, P., Ritz, T., Burda, H., Wegner, R.E., Wiltschko, R., 2006. The magnetic compass mechanisms of birds and rodents are based on different physical principles. J. R. Soc. Interface 3, 583–587. Treiber, C.D., Salzer, M.C., Riegler, J., Edelman, N., Sugar, C., Breuss, M., Pichler, P., Cadiou, H., Saunders, M., Lythgoe, M., Shaw, J., Keays, D.A., 2012. Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484, 367–370. Vácha, M., Kvicalova, M., Puzova, T., 2010. American cockroaches prefer four cardinal geomagnetic positions at rest. Behaviour 147, 425–440. Vargas, J.P., Siegel, J.J., Bingman, V.P., 2006. The effects of a changing ambient magnetic field on single-unit activity in the homing pigeon hippocampus. Brain
147
Res. Bull. 70, 158–164. Walker, S.F., 1980. Lateralization of functions in the vertebrate brain: a review. Br. J. Psychol. 71, 329–367. Wendt, P.E., Risberg, J., 1994. Cortical activation during visual spatial processing: Relation between hemispheric asymmetry of blood flow and performance. Brain Cogn. 24, 87–103. Wiltschko, R., Wiltschko, W., 2012. Magnetoreception, Sensing in Nature. Springer, pp. 126–141. Wiltschko, R., Stapput, K., Ritz, T., Thalau, P., Wiltschko, W., 2007. Magnetoreception in birds: different physical processes for two types of directional responses. Hum. Front. Sci. Program J. 1, 41–48. Wiltschko, W., Wiltschko, R., 1972. Magnetic compass of European robins. Science 176, 62–64. Wiltschko, W., Wiltschko, R., 2007. Magnetoreception in birds: two receptors for two different tasks. J. Ornithol. 148, S61–S76. Wiltschko, W., Munro, U., Ford, H., Wiltschko, R., 2003. Lateralisation of magnetic compass orientation in silvereyes, Zosterops lateralis. Aust. J. Zool. 51, 597–602. Wiltschko, W., Traudt, J., Güntürkün, O., Prior, H., Wiltschko, R., 2002. Lateralization of magnetic compass orientation in a migratory bird. Nature 419, 467–470. Wilzeck, C., Wiltschko, W., Güntürkün, O., Wiltschko, R., Prior, H., 2010. Lateralization of magnetic compass orientation in pigeons. J. R. Soc. Interface 7 (Suppl. 2), S235–S240. Wu, L.-Q., Dickman, J.D., 2011. Magnetoreception in an avian brain in part mediated by inner ear lagena. Curr. Biol. 21, 418–423. Wu, L.Q., Dickman, J.D., 2012. Neural correlates of a magnetic sense. Science 336, 1054. Zapka, M., Heyers, D., Hein, S., Engels, S., Schneider, N.L., Hans, J., Weiler, S., Dreyer, D., Kishkinev, D., Wild, J.M., Mouristen, H., 2009. Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461, 1274–1277.
Contents lists available at ScienceDirect
Journal of Theoretical Biology journal homepage: www.elsevier.com/locate/yjtbi
Shifted magnetic alignment in vertebrates: Evidence for neural lateralization? E. Pascal Malkemper a,b, Michael S. Painter c, Lukas Landler c,d,n a
Department of General Zoology, Faculty of Biology, University of Duisburg-Essen, Universitätsstrasse. 2, 45117 Essen, Germany Department of Game Management and Wildlife Biology, Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, Kamýcká 129, 165 21 Prague 6, Czech Republic c Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia, United States of America d Research Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), 1030 Vienna, Austria b
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
Many vertebrate taxa consistently align along the magnetic northsouth axis. Meta-analysis shows a consistent mean clockwise rotation from magnetic north-south. Consistent shift may be due to lateralized magnetic processing in the nervous system.
art ic l e i nf o
a b s t r a c t
Article history: Received 5 January 2016 Received in revised form 13 March 2016 Accepted 28 March 2016 Available online 6 April 2016
A wealth of evidence provides support for magnetic alignment (MA) behavior in a variety of disparate species within the animal kingdom, in which an animal, or a group of animals, show a tendency to align the body axis in a consistent orientation relative to the geomagnetic field lines. Interestingly, among vertebrates, MA typically coincides with the north–south magnetic axis, however, the mean directional preferences of an individual or group of organisms is often rotated clockwise from the north–south axis. We hypothesize that this shift is not a coincidence, and future studies of this subtle, yet consistent phenomenon may help to reveal some properties of the underlying sensory or processing mechanisms, that, to date, are not well understood. Furthermore, characterizing the fine structure exhibited in MA behaviors may provide key insights to the biophysical substrates mediating magnetoreception in vertebrates. Therefore, in order to determine if a consistent shift is exhibited in taxonomically diverse vertebrates, we performed a meta-analysis on published MA datasets from 23 vertebrate species that exhibited an axial north–south preference. This analysis revealed a significant clockwise shift from the north–south magnetic axis. We summarize and discuss possible competing hypotheses regarding the proximate mechanisms underlying the clockwise shifted MA and conclude that the most likely cause of such a shift would be a lateralization in central processing of magnetic information. & 2016 Elsevier Ltd. All rights reserved.
Keywords: Magnetoreception Magnetic alignment Lateralization Geomagnetic field Cortical hemispheres Spatial orientation Central sensory processing
1. Background
n
Corresponding author. E-mail address: [email protected] (L. Landler).
http://dx.doi.org/10.1016/j.jtbi.2016.03.040 0022-5193/& 2016 Elsevier Ltd. All rights reserved.
Many animals use the Earth's magnetic field to orient in their environment (Wiltschko and Wiltschko, 2012). For instance, migrating birds use a magnetic compass during seasonal migrations
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(Wiltschko and Wiltschko, 1972), hatchling sea turtles use navigational markers provided by components of the Earth's magnetic field to guide innate migration along the Atlantic gyre (Lohmann et al., 2012), and newts possess a magnetic compass and a magnetic map which is used during navigation (Phillips et al., 2002a). In addition to the so-called ‘goal oriented’ magnetic behaviors, many animals show spontaneous magnetic responses (Begall et al., 2013), often referred to as ‘magnetic alignment’ (MA). As used in this article, MA describes a spontaneous, non-goal directed magnetic response, such as the tendency of animals to spontaneously align their body axis relative to the Earth's magnetic field. Magnetic alignment was first described over 50 years ago in insects (i.e. in European cockchafer, Melolontha melolontha, (Schneider, 1963)), and today evidence suggests that this behavior is commonplace among animals across diverse taxa (Begall et al., 2013). However, although widespread within the animal kingdom, little is known about the sensory mechanisms and the functional significance of MA behaviors. Insects often exhibit quadrimodal spontaneous orientation, aligning along cardinal or anticardinal magnetic axes, (Becker et al., 1996, 1964; Becker and Speck, 1964; Painter et al., 2013; Vácha et al., 2010), whereas vertebrates show preferences to align their body along the north–south magnetic axis (Begall et al., 2008, 2011; Burda et al., 2009; Hart et al., 2012, 2013a, 2013b; Slaby et al., 2013). The same directional tendencies have been shown in spontaneous directional nest construction of some mammals when tested in visually symmetric circular arenas (Malkemper et al., 2015; Oliveriusová et al., 2014). Even though it is controversial whether nest-building preferences represent a form of magnetic alignment equivalent to the alignment behaviors discussed above [see (Begall et al., 2013)], in the current discussion they are considered spontaneous directional responses to the geomagnetic field, and therefore are included in our definition and analysis. Few studies have attempted to investigate the magnetoreception mechanism underlying MA. While subterranean rodents (mole-rats) seem to use a magnetite-based mechanism (MBM) (Marhold et al., 1997; Thalau et al., 2006), evidence from other vertebrates, including epigeic mammals, points towards the involvement of a radical pair mechanism (RPM) (Landler et al., 2015; Malkemper et al., 2015). The RPM has also been implicated in the magnetic compass response of migratory birds and amphibians (Phillips et al., 2010b; Ritz, 2011). However, strong support for a magnetite-based mechanism mediating spontaneous nest building responses comes from mole-rats, the best studied group of mammals for magnetoreception to date. It is, however, unclear whether this represents the general mechanism underlying all vertebrate magnetoreception, or rather, if mole-rats represent the exception to the rule given their unique subterranean lifestyle. Birds and newts seem to possess both types of receptors used for different tasks (Phillips, 1986; Wiltschko et al., 2007). While the underlying mechanisms of MA are poorly understood, even less evidence exists concerning its possible function and biological significance (Begall et al., 2013). The only study linking MA behavior to a biological fitness advantage showed that red foxes were approximately 60 70% more successful at catching hidden prey when mousing jumps were directed towards northeast or south-west, compared to mousing attempts in other magnetic directions (Červený et al., 2011). This observation fits quite well with the idea that animals use a visual pattern that receives input from the geomagnetic field to encode their environment (Phillips et al., 2010a). A biophysical mechanism that creates such a visual pattern has been suggested to underlie magnetic compass responses in a variety of vertebrates (Cintolesi et al., 2003; Ritz et al., 2000), and has been proposed to be generated through a radical pair mechanism (RPM) occurring in specialized photoreceptors of the retina or pineal organ (Hart et al.,
2013a, 2013b; Nießner et al., 2011; Phillips et al., 2010a, 2001). Behavioral evidence from turtles suggests that the same RPM pattern might be involved in encoding novel environments, where an association is formed between novel places and a particular ‘visual’ pattern (Landler et al., 2015). In the case of mousing red foxes, the visual pattern generated from an RPM might act as a range finder helping to estimate prey distances and/or guide the trajectory of the jump (Červený et al., 2011) in a similar way as the patterns has been proposed to facilitate the tendency of waterfowl landing along the north–south magnetic axis (Hart et al., 2013a, 2013b). Interestingly, in cases where animals align axially along the north–south axis, as is the case in most vertebrates, but also reported in some invertebrates (Sandoval et al., 2012), there tends to be a conspicuous shift of the mean alignment clockwise from the magnetic north–south axis. A consistent shift across multiple species during various behaviors (e.g. grazing, sleeping, landing, hunting, nest building) would not be predicted from the hypotheses for the biological function or the underlying receptor mechanism of MA that have been proposed to date. However, such a phenomenon in spatial behaviors might indicate a functional lateralization of the underlying magnetic sensory pathway in vertebrates, as has been suggested in different species of migratory birds but remains a highly debated topic in magnetoreception. While research in different bird species provided evidence for a lateralized magnetic compass located in the right eye (Wiltschko et al., 2002), later evidence challenged these results, possibly suggesting a more complex story involving developmental effects on the underlying sensory mechanism (Gehring et al., 2012; Hein et al., 2011). It is further likely, that there exists a functional lateralization rather than an absolutely lateralized receptor distribution with regard to the magnetic sense, as was deduced from experiments with birds showing ocular dominance, predominantly using one eye over the other depending on the type of magnetic tasks (Wilzeck et al., 2010). Such a functional lateralization might be related to the widespread lateralized central processing of information in vertebrate brains (Halpern et al., 2005; Walker, 1980). Current knowledge about central processing of magnetic information in the brain of vertebrates is limited and mostly based on studies of immediate early gene expression induced by magnetic stimulation (see discussion for details). Based on the findings in birds, two pathways processing magnetic information have been suggested, one for each receptor type (MBM and RPM) (Mouritsen et al., 2015). The pathway for magnetic compass information (mediated by RPM) in the bird brain connects the primary receptors that are believed to reside in the retina via the dorsal lateral geniculate nucleus of the thalamus to the forebrain Cluster N and adjacent hyperpallial areas (Mouritsen et al., 2015). Magnetic map information (mediated by MBM) on the other hand is suggested to be routed via trigeminal brainstem nuclei to the forebrain nucleus basalis and trigeminal parts of the nidopallium (Mouritsen et al., 2015). If these two pathways mediating magnetic information were anatomically and/or functionally lateralized, it would be conceivable that the lateralization results in shifted MA behavior, which could in turn shed light on the enigmatic biological function of vertebrate MA. Here, we performed a meta-analysis of published data after a systematic literature search on vertebrate axial MA responses addressing two main questions: (1) Do mean responses from vertebrate species show a consistent and significant clockwise shift, deviating from the magnetic north–south axis, and (2) what are possible explanations for such a shift in light of evidence on the underlying mechanism and possible adaptive functions?
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2. Method 2.1. Data collection We collected axial MA data of 23 vertebrate species that have been published or have been submitted to a peer-reviewed journal. All species for which data were available are listed in Table 1. Our criteria for inclusion of data were the following: axial response of vertebrate species (excluding unimodal and quadrimodal responses) under natural (full spectrum) light conditions and the data is presented with unweighted data points. We classified distributions according to the difference of their mean vector from pointing towards magnetic north, i.e. 0°, as being either clockwise shifted (1–45°), or counterclockwise shifted (315–0°). Zero degree (0°) was categorized as counterclockwise in order to avoid any bias in favor of our hypothesis. Data from trained assays were excluded from the analysis although, in some cases, spontaneous responses emerged (Muheim et al., 2006). 2.2. Analysis We used the non-parametric exact binominal test (two-tailed) to analyze if the proportion of alignment responses between clockwise and counterclockwise was different from the 0.5 level of chance that would be expected if the animals show no consistent departure from the north–south axis. Furthermore, we combined all available data on axial vertebrate alignment and calculated the mean alignment across studies using Rayleigh test. We calculated the 95% confidence interval in order to test if magnetic north was included in the mean direction. The statistical software R (R Development Core Team, 2012) was used for linear statistics and Oriana 4.02 was used for circular statistics (Kovach, 2011).
3. Results Our literature survey, including data submitted for publication, revealed data sets for axial vertebrate alignment from 10 studies including 23 different species (Table 1). The proportion of CW alignment responses was 0.78, and the exact binominal test
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showed that the proportion of CW to CCW studies was significantly different from the 0.5 chance level (p ¼0.01), suggesting a significant clockwise shift in axial alignment responses. All literature accounts combined showed a highly significant axial alignment towards 9.1°/189.1° (Rayleigh test p o0.0001, r ¼0.931), and the 95% confidence interval did not include magnetic north (4.6–13.5°/184.6–193.5°; see Fig. 1).
4. Discussion The presented data provide evidence for a consistent shift in vertebrate magnetic alignment behavior that deviates significantly clockwise from magnetic north. Not only is it intriguing that such a diverse range of species show axially symmetrical spatial behavior aligned spontaneously along the north–south magnetic axis, but also that a consistent clockwise shift seems to be ubiquitous across vertebrates exhibiting axial MA behavior, and could be interpreted as evidence for similarity of the underlying sensory mechanism and/or its adaptive functionality. The deviation from the magnetic north–south axis could originate at different levels in the sensory hierarchy: (1) it could be related to asymmetries at the receptor level, or (2) to functional brain asymmetries, i.e. central processing. We will discuss both possibilities below. 4.1. Asymmetries at the receptor level Although the exact nature of animal magnetoreceptors is still unknown, the results of several behavioral experiments with migratory birds suggest that magnetic compass responses are mediated by the eyes, and there is evidence that this processes may be lateralized, located in the right eye (Gehring et al., 2012; Wiltschko et al., 2003; Wiltschko et al., 2002). This lateralization of magnetic compass responses, which is thought to be mediated by a ‘light-dependent’ magnetoreceptor, was, however, heavily discussed and claimed not to be a common feature in birds (Hein et al., 2011, 2009). It is unclear if lateralization at the receptor level is a general feature across all vertebrates, but if so, it could contribute to lateralized magnetic behaviors, such as the shift in MA presented here. Animals may tend to center, or align such a
Table 1 Collection of literature data included in the study. Only data sets with statistically significant axial mean directions (Rayleigh test) were included. We defined only mean axial directions (Mean dir.) between 1° and 45° as being clockwise-shifted ('CW-shift'). Author
Year
Phillips et al. (2002b) Hart et al. (2012a, 2013b) Begall et al. (2008) Begall et al. (2008) Begall et al. (2008) Červený et al. (2016) Červený et al. (2016) Oliveriusová et al. (2014) Malkemper et al. (2015) Kušta et al. (in preparation) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b) Hart et al. (2013a, 2013b)
Class
Order
Species
Location
Mean dir. (deg)
CW-shift
Amphibia Teleostei Mammalia
Caudata Cypriniformes Artiodactyla
Notophthalmus viridescens Cyprinus carpio Cervus elaphus Capreolus capreolus Bos primigenius Sus scrofa Phacochoerus africanus Clethrionomys glareolus Apodemus sylvaticus Lepus europaeus Alopochen aegyptiacus Anas penelope Anas platyrhynchos Aythya ferina Cygnus olor Dendrocygna viduata Larus canus Larus ridibundus Mergellus albellus Mergus merganser Nettapus auritus Vanellus armatus Vanellus coronatus
USA Czech Republic Global Global Global Czech Republic South Africa Czech Republic Czech Republic Czech Republic Botswana Finland Europe, North-America Poland Europe Botswana Finland Europe Finland Finland Botswana Botswana Botswana
38 8 10 9 6 17 25 0 23 15 175 7 9 8 3 4 6 19 3 5 176 177 179
Yes Yes Yes Yes Yes Yes Yes No Yes Yes No Yes Yes Yes Yes Yes Yes Yes Yes Yes No No No
Rodentia
Aves
Lagomorpha Anseriformes
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Fig. 1. Mean axial orientations of 23 different vertebrate species. The two-headed arrow represents the mean vector (mean direction: 9°/189°); the arrow length is proportional to the mean vector length (r ¼0.931), with the radius of the circle equal to 1 (i.e. r ¼ 1). Each pair of opposite symbols represents the mean axial orientation of one alignment study. The dotted circle represents the threshold for a mean vector length that would result in p ¼ 0.001. Dotted lines represent the 95% confidence interval around the mean (4.6–13.5°/184.6–193.5°). Data are plotted relative to magnetic north.
lateralized receptor system (e.g. right or left eye) with the north– south axis/field lines (i.e. most salient reference point) resulting in a slightly shifted body axis of the individual relative to the magnetic field lines (all species included in the analysis have laterally positioned eyes). From physical models it can be adduced that the visual pattern produced by the hypothesized RPM could be realized as an axially symmetrical pattern at the sensory level, e.g. visual system (Ritz et al., 2000; Solov'yov et al., 2010). In the proposed models, the north–south axis of the geomagnetic field constitutes the major axis of this pattern. If central parts of that pattern (i.e. the strongest/weakest signal of the pattern) provide a more salient spatial cue for navigation or MA behaviors (Begall et al., 2013; Phillips et al., 2010a), aligning lateralized receptors would result in a slightly shifted alignment of the axis of the organism with respect to the magnetic field lines. Interestingly, the photoreceptor distribution in some birds shows slight differences between the left and the right eye (Hart, 2001). The left eye possesses more single cones which are important for spectral discrimination and high visual acuity, while the right eye possesses more double-cones which are essential for the detection of motion. Although the differences are small, they are associated with a clear behavioral lateralization (Güntürkün et al., 2000), and therefore provide the possibility that a similar lateralization may underlie MA behaviors. Cryptochromes, blue-light sensitive flavoproteins, have been proposed as the putative magnetoreceptor molecules mediating a RPM in invertebrates and vertebrates, because their spectral and chemical properties fit with most behavioral and histological evidence (Dodson et al., 2013). In birds, one type of cryptochrome, cryptochrome 1a, is present in the outer segments of all cones that contain opsins sensitive to light in the ultraviolet spectrum (UV cones). This is consistent with theoretical proposals for an involvement of cryptochrome 1a in creating a magnetic visual pattern (Nießner et al., 2011). Interestingly, these cryptochromecontaining UV cones have been shown to be up to 20% more abundant in the left eye of the European starling than in the right eye (Hart et al., 2000a). This might indicate that also cryptochrome 1a is asymmetrically distributed. The only additional quantitative study on bilateral photoreceptor distribution was done on blue tits and blackbirds, where UV cones were not found in significantly
higher densities in the left eye (Hart et al., 2000b). However, it has been argued that several mammal species, despite showing clear MA (e.g. ungulates), do not express cryptochrome 1 in their blue cones (homologous to avian UV cones, Nießner et al. (2016)) Therefore, with the exception of European starlings, the data available does not support an asymmetric cryptochrome distribution providing the basis for the MA-shift. Clearly, future histological studies of cryptochrome's distribution across species in different seasonal, physiological and developmental states will provide additional support for, or against, the role of lateralization underlying MA behavior. Finally, newts, which also show a clockwise shifted MA, appear to have their light dependent magnetoreceptor in the parietal eye, a homolog to the pineal organ of other vertebrates, rather than the retina (Deutschlander et al., 1999). This organ is unpaired, and consequently has no conceivable lateralization. Therefore, if the consistent shift in MA results from a common factor across all species, a functional lateralization at the RPM receptor-level is unlikely to be the cause. Another idea that can be related to receptor lateralization was proposed by Phillips et al. (2002b) and assumes a magnetite-based magnetoreceptor (MBM) underlying MA, or a combination of MBM and the previously mentioned RPM. Magnetite-based magnetoreception is an alternative mechanism to the RPM, where magnetite particles are thought to provide the animals with a magnetometer and/or magnetic compass (Kirschvink et al., 2001). For most epigeic vertebrates studied so far it is assumed that they possess both magnetoreceptors (RPM and MBM), with the RPM providing a magnetic compass and the MBM providing magnetic ‘map’ information (magnetic latitudinal or longitudinal position may be derived using spatial gradients, e.g. intensity and/or inclination, provided by the magnetic field) (Phillips, 1986; Wiltschko and Wiltschko, 2007). In order to perceive a consistent and comparable 'map reading', the animals would reduce variation in the magnetic measurements by rotating the receptor towards a consistent alignment, likely using the magnetic field lines to guide this alignment behavior. They might achieve this by using the RPM compass to align the map receptor with respect to the field lines and then take the reading (Phillips et al., 2002b). A lateralized magnetite based map detector could theoretically cause a corresponding shift of the alignment axis. In fact, measurements of the natural remanent magnetism (NRM) of 18 newts showed individual differences in the NRM declination (in relation to the newts' body axis). Furthermore, when tested under full spectrum light, the NRM declinations seemed to correlate with the newts' alignment responses (Phillips et al., 2002b). However, it is unclear if the NRM declination is related to a magnetite receptor at this stage of the research. Phillips et al. (2002b) also proposed that the alignment they found under long-wavelength, where the RPM system is not expected to function, is based on a ‘systematic sampling strategy’ to find the alignment of the ‘map receptor’ and therefore the reliable map reading. It is worth noting that also under such long-wavelength conditions, which are not included in this current meta-analysis, the alignment was shifted clockwise. Further studies would be needed to determine if magnetite is generally involved in MA and if there is a general directional bias in magnetite receptors. In addition, because of recent failures to locate a MBM (Edelman et al., 2015; Treiber et al., 2012), such questions might remain unexplored until a vertebrate MBM is confirmed by histological studies. 4.2. Asymmetries at the level of the central nervous system It is well established that many animals show lateralized control of a great variety of different behaviors (reviewed in Duboc et al., 2015; Rogers and Andrew, 2002). Such lateralization can differ between individuals (individual bias) or be consistent within
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a whole population (population wide bias). Only a population wide bias that extends across species could explain the consistent shift in MA. Behavioral lateralization is based on specialization of the cortical hemispheres or unilateral nerve centers to accomplish certain tasks, which are then not directly fulfilled by the contralateral equivalent. Consequently, behaviors become lateralized as many motor systems and many sensory organs are unilaterally innervated. Below we will give some examples and discuss how they could explain the MA shift. In many vertebrates, dominance of one hemisphere during certain behaviors is expressed in a predominant use of a single eye during a particular task. The left eye has been shown to be especially important during the visual assessment of space, especially for the use of distant visual features for orientation and the detection of threats (Duboc et al., 2015; Rogers and Andrew, 2002). Such visuospatial right-hemispheric dominance seems to be a general vertebrate trait as it has been well documented in birds (McKenzie et al., 1998; Rashid and Andrew, 1989), cattle (Robins and Phillips, 2010), rodents (Cowell et al., 1997), and primates including humans (Hopkins and Morris, 1989; Wendt and Risberg, 1994). It has been argued that the cryptochrome-based magnetic field perception (mediated by a RPM) serves as a visual grid that helps to put landmarks into global perspective (Phillips et al., 2010a). It is reasonable to assume that the central axis of this symmetrical pattern would be predominantly perceived via the eye that is specialized on spatial tasks; the left eye in vertebrates (see above). Correspondingly, in magnetic conditioning experiments it has been demonstrated that pigeons use the right eye for goal-directed determination of magnetic compass directions while usage of the left eye led to axial responses (Wilzeck et al., 2010). The left eye seems to be preferred during non-goal directed tasks, such as spontaneous magnetic alignment and would help to explain the clockwise shift, if the left eye was aligned with magnetic north. Thus, it is conceivable that the clockwise shift observed in MA studies is based on a lateralized higher processing of magnetic information. Unfortunately, the neuronal processes underlying magnetic orientation are still unclear. A number of studies in bird and rodent species have shown activation of certain brain regions in response to magnetic stimuli; usually immediate early genes are used as correlates for neuronal activation (i.e. ZENK (Heyers et al., 2007, 2010; Lefeldt et al., 2014; Liedvogel et al., 2007; Mouritsen et al., 2005; Shimizu et al., 2004) and c-fos (Burger et al., 2010; Němec et al., 2001; Wu and Dickman, 2011)). Electrophysiological methods have also revealed neuronal responses to magnetic field changes (Semm and Demaine, 1986; Semm and Beason, 1990; Semm et al., 1984; Vargas et al., 2006; Wu and Dickman, 2012, but see Ramírez et al., 2014). In birds, brain regions involved in magnetoreception seem to be brainstem nuclei of the trigeminal and vestibular system as well as the hippocampus (Lefeldt et al., 2014; Semm et al., 1984; Wu and Dickman, 2011). Furthermore, a specific region of the bird forebrain (Cluster N) is crucial for magnetic orientation in night migrants, although its functional role within the system is unknown (Mouritsen et al., 2005; Zapka et al., 2009). In mammals, magnetic activation has been detected in the hippocampus, the superior colliculus and the primary somatosensory cortex (Burger et al., 2010; Němec et al., 2001). In many studies, neuronal activation in response to magnetic fields has been found bilaterally without evidence of lateralization (reviewed in Mouritsen and Hore, 2012). This does, however, not dissent with the idea of a task-dependent lateralization of magnetic behaviors as it is suggested by the findings of Wilzeck et al. (2010). For example, none of the neuronal activations studies used magnetic alignment to induce neuronal activity. Furthermore, when it was specifically
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addressed, a significant left eye/right hemisphere dominance was demonstrated within Cluster N during a magnetic orientation task in European robins and two warbler species (Liedvogel et al., 2007). Further detailed investigations of lateralization in all parts of the central pathway of magnetic information during different magnetic tasks is clearly needed (see Wilzeck et al., 2010). Finally, lateralized processing of magnetic information does not necessarily lead to lateralized activation of primary magnetoreceptive areas, but might be confined to higher order association areas. 4.3. Conclusion Following an a priori established criteria, our meta-analysis shows a highly significant magnetic alignment across vertebrate species along the north–south axis. However, a consistent clockwise shift from the exact north–south axis is an evident and intriguing feature of this behavior and is consistent across multiple vertebrate species. One could argue that such a consistent bias could provide insights into the underlying physiological mechanism of magnetoreception. We theorized that a bias could, in principle, originate at two different, but not necessarily exclusive, levels: asymmetries at the receptor level, or of central processing. Evidence for or against lateralization of the magnetoreceptors is currently weak and progress is hampered by the fact that the magnetoreceptors are still unknown. For the most probable candidate, cryptochrome 1, weak evidence for lateralization exists, but without further and stronger evidence it is difficult to argue that a cryptochrome asymmetry is responsible for the MA shift. On the other hand, behavioral lateralization has been conclusively and consistently shown among several vertebrate orders and the proposed functional asymmetry between the left and right eye is in line with a hypothetical spatial function of RPM-based magnetoreceptors. Thus, we conclude that a general lateralization of the central nervous system, which has been found to be a common vertebrate trait, is the most probable origin of the MA-shift. However, the presented paper should be seen as a thoughtprovoking and hypothesis-generating analysis, hopefully encouraging new research leading to a deeper understanding of spontaneous magnetic preferences in animals. Therefore, we conclude this paper by posing three essential questions that should be addressed in future research on vertebrate magnetic alignment: 1. What is the magnetoreception mechanism underlying magnetic alignment (RPM and/or MBM)? 2. Is the MA-shift lost or reverted when the left eye is covered? 3. What is the adaptive significance of MA, e.g. is it involved in the calibration/reading of a magnetic map and/or does it have a role in magnetic navigation?
Acknowledgments This research was supported by the Grant Agency of the Czech Republic (Project no. 15-21840S to EPM). We thank Sabine Begall, Hynek Burda, Sara-Maria Schnedl and three anonymous reviewers for valuable comments on earlier versions of the manuscript.
References Becker, E., Hemmersbach, R., Stockem, W., 1996. Einfluss niederfrequenter Magnetfelder auf das Orientierungsverhalten von Einzellern: Neue Erkenntnisse zur biologischen Wirkung elektromagnetischer Wechselfelder. DLR Nachrichten
146
E.P. Malkemper et al. / Journal of Theoretical Biology 399 (2016) 141–147
81, 22–26. Becker, G., 1964. Reaktion von Insekten auf Magnetfelder, elektrische Felder und atmospherics. Z. für Angew. Èntomol. 54, 75–88. Becker, G., Speck, U., 1964. Untersuchungen über die Magnetfeld-Orientierung von Dipteren. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 49, 301–340. Begall, S., Červený, J., Neef, J., Vojtěch, O., Burda, H., 2008. Magnetic alignment in grazing and resting cattle and deer. Proc. Natl. Acad. Sci. 105, 13451–13455. Begall, S., Malkemper, E.P., Červený, J., Němec, P., Burda, H., 2013. Magnetic alignment in mammals and other animals. Mamm. Biol. 78, 10–20. Begall, S., Burda, H., Červený, J., Gerter, O., Neef-Weisse, J., Němec, P., 2011. Further support for the alignment of cattle along magnetic field lines: reply to Hert et al. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol., 1–7. Burda, H., Begall, S., Červený, J., Neef, J., Němec, P., 2009. Extremely low-frequency electromagnetic fields disrupt magnetic alignment of ruminants. Proc. Natl. Acad. Sci. 106, 5708–5713. Burger, T., Lucová, M., Moritz, R.E., Oelschläger, H.H.A., Druga, R., Burda, H., Wiltschko, W., Wiltschko, R., Němec, P., 2010. Changing and shielded magnetic fields suppress c-Fos expression in the navigation circuit: input from the magnetosensory system contributes to the internal representation of space in a subterranean rodent. J. R. Soc. Interface 7, 1275–1292. Červený, J., Begall, S., Koubek, P., Nováková, P., Burda, H., 2011. Directional preference may enhance hunting accuracy in foraging foxes. Biol. Lett. 7, 355–357. Červený J., Burda H., Ježek M., Kušta T., Husinec V., Nováková P., Hart V., Hartová V., Begall S. and Malkemper E.P., 2016. Magnetic alignment in wild boars (Sus scrofa) and warthogs (Phacochoerus africanus). Mammal Review, in press. Cintolesi, F., Ritz, T., Kay, C.W.M., Timmel, C.R., Hore, P.J., 2003. Anisotropic recombination of an immobilized photoinduced radical pair in a 50-[mu] T magnetic field: a model avian photomagnetoreceptor. Chem. Phys. 294, 385–399. Cowell, P., Waters, N., Denenberg, V., 1997. The effects of early environment on the development of functional laterality in Morris maze performance. Laterality: asymmetries of body. Brain Cogn. 2, 221–232. Deutschlander, M.E., Borland, S.C., Phillips, J.B., 1999. Extraocular magnetic compass in newts. Nature 400, 324–325. Dodson, C.A., Hore, P.J., Wallace, M.I., 2013. A radical sense of direction: signalling and mechanism in cryptochrome magnetoreception. Trends Biochem. Sci. 38, 435–446. Duboc, V., Dufourcq, P., Blader, P., Roussigné, M., 2015. Asymmetry of the brain: development and implications. Annu. Rev. Genet. 49, 647–672. Edelman, N.B., Fritz, T., Nimpf, S., Pichler, P., Lauwers, M., Hickman, R.W., PapadakiAnastasopoulou, A., Ushakova, L., Heuser, T., Resch, G.P., Saundersd, M., Shawd, J.A., Keays, D.A., 2015. No evidence for intracellular magnetite in putative vertebrate magnetoreceptors identified by magnetic screening. Proc. Natl. Acad. Sci. 112, 262–267. Gehring, D., Wiltschko, W., Güntürkün, O., Denzau, S., Wiltschko, R., 2012. Development of lateralization of the magnetic compass in a migratory bird. Proc. R. Soc. B: Biol. Sci. 282, 1–6. Güntürkün, O., Diekamp, B., Manns, M., Nottelmann, F., Prior, H., Schwarz, A., Skiba, M., 2000. Asymmetry pays: visual lateralization improves discrimination success in pigeons. Curr. Biol. 10, 1079–1081. Halpern, M.E., Güntürkün, O., Hopkins, W.D., Rogers, L.J., 2005. Lateralization of the vertebrate brain: taking the side of model systems. J. Neurosci. 25, 10351–10357. Hart, N., Partridge, J., Cuthill, I., 2000a. Retinal asymmetry in birds. Curr. Biol. 10, 115–117. Hart, N., Partridge, J., Cuthill, I., Bennett, A.T., 2000b. Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.). J. Comp. Physiol. A 186, 375–387. Hart, N.S., 2001. The visual ecology of avian photoreceptors. Progress Retin. Eye Res. 20, 675–703. Hart, V., Malkemper, E.P., Kušta, T., Begall, S., Nováková, P., Hanzal, V., Pleskač, L., Ježek, M., Policht, R., Husinec, V., 2013a. Directional compass preference for landing in water birds. Front. Zool. 10, 38. Hart, V., Novakova, P., Malkemper, E.P., Begall, S., Hanzal, V., Jezek, M., Kusta, T., Nemcova, V., Adamkova, J., Benediktova, K., Červený, J., Burda, H., 2013b. Dogs are sensitive to small variations of the Earth's magnetic field. Front. Zool. 10, 80. Hart, V., Kusta, T., Nemec, P., Blahova, V., Jezek, M., Novakova, P., Begall, S., Cerveny, J., Hanzal, V., Malkemper, E.P., Stipek, K., Vole, C., Burda, H., 2012. Magnetic alignment in carps: evidence from the Czech christmas fish market. PLoS One 7, e51100. Hein, C.M., Engels, S., Kishkinev, D., Mouritsen, H., 2011. Robins have a magnetic compass in both eyes. Nature 471, E1. Hein, C.M., Zapka, M., Heyers, D., Kutzschbauch, S., Schneider, N.-L., Mouritsen, H., 2009. Night-migratory garden warblers can orient with their magnetic compass using the left, the right or both eyes. J. R. Soc. Interface, 20090376. Heyers, D., Manns, M., Luksch, H., Güntürkün, O., Mouritsen, H., 2007. A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLoS One 9, e937. Heyers, D., Zapka, M., Hoffmeister, M., Wild, J., Mouritsen, H., 2010. Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. Proc. Natl. Acad. Sci. USA 107, 9394–9399. Hopkins, W.D., Morris, R.D., 1989. Laterality for visual-spatial processing in two language-trained chimpanzees (Pan troglodytes). Behav. Neurosci. 103, 227. Kirschvink, J.L., Walker, M.M., Diebel, C.E., 2001. Magnetite-based
magnetoreception. Curr. Opin. Neurobiol. 11, 462–467. Kovach, W.L., 2011. Oriana – Circular Statistics for Windows Ver. 4. Kovach Computing Services, Pentraeth, Wales, UK. Kušta T., Červený J., Ježek M., Koubek P., Begall S., Malkemper E.P. and Burda H., Magnetic alignment in European hares (Lepus europaeus). In preparation. Landler, L., Painter, M.S., Youmans, P.W., Hopkins, W.A., Phillips, J.B., 2015. Spontaneous magnetic alignment by yearling snapping turtles: rapid association of radio frequency dependent pattern of magnetic input with novel surroundings. PLoS One 10, e0124728. Lefeldt, N., Heyers, D., Schneider, N.-L., Engels, S., Elbers, D., Mouritsen, H., 2014. Magnetic field-driven induction of ZENK in the trigeminal system of pigeons (Columba livia). J. R. Soc. Interface 11. Liedvogel, M., Feenders, G., Wada, K., Troje, N.F., Jarvis, E.D., Mouritsen, H., 2007. Lateralized activation of cluster N in the brains of migratory songbirds. Eur. J. Neurosci. 25, 1166–1173. Lohmann, K.J., Putman, N.F., Lohmann, C.M.F., 2012. The magnetic map of hatchling loggerhead sea turtles. Curr. Opin. Neurobiol. 22, 336–342. Malkemper, E.P., Eder, S.H.K., Begall, S., Phillips, J.B., Winklhofer, M., Hart, V., Burda, H., 2015. Magnetoreception in the wood mouse (Apodemus sylvaticus): influence of weak frequency-modulated radio frequency fields. Sci. Rep., 4. Marhold, S., Wiltschko, W., Burda, H., 1997. A magnetic polarity compass for direction finding in a subterranean mammal. Naturwissenschaften 84, 421–423. McKenzie, R., Andrew, R.J., Jones, R.B., 1998. Lateralisation in chicks and hens: new evidence for control of response by the right eye system. Neuropsychologia 36, 51–58. Mouritsen, H., Hore, P.J., 2012. The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds. Curr. Opin. Neurobiol. 22, 343–352. Mouritsen, H., Heyers, D., Güntürkün, O., 2015. The neural basis of long-distance navigation in birds. Annu. Rev. Physiol. Mouritsen, H., Feenders, G., Liedvogel, M., Wada, K., Jarvis, E.D., 2005. Night-vision brain area in migratory songbirds. Proc. Natl. Acad. Sci. USA 102, 8339–8344. Muheim, R., Edgar, N.M., Sloan, K.A., Phillips, J.B., 2006. Magnetic compass orientation in C57BL/6J mice. Learn. Behav. 34, 366–373. Němec, P., Altmann, J., Marhold, S., Burda, H., Oelschläger, H.H., 2001. Neuroanatomy of magnetoreception: the superior colliculus involved in magnetic orientation in a mammal. Science 294, 366–368. Nießner, C., Denzau, S., Malkemper, E.P., Gross, J.C., Burda, H., Winklhofer, M., Peichl, L., 2016. Cryptochrome 1 in retinal cone photoreceptors suggests a novel functional role in mammals. Sci. Rep. 6, 21848. Nießner, C., Denzau, S., Gross, J.C., Peichl, L., Bischof, H.-J., Fleissner, G., Wiltschko, W., Wiltschko, R., 2011. Avian ultraviolet/violet cones identified as probable magnetoreceptors. PLoS One 6, e20091. Oliveriusová, L., Němec, P., Pavelková, Z., Sedláček, F., 2014. Spontaneous expression of magnetic compass orientation in an epigeic rodent: the bank vole, Clethrionomys glareolus. Naturwissenschaften 101, 557–563. Painter, M.S., Dommer, D.H., Altizer, W.W., Muheim, R., Phillips, J.B., 2013. Spontaneous magnetic orientation in larval Drosophila shares properties with learned magnetic compass responses in adult flies and mice. J. Exp. Biol. 216, 1307–1316. Phillips, J.B., 1986. Two magnetoreception pathways in a migratory salamander. Science 233, 765–767. Phillips, J.B., Muheim, R., Jorge, P.E., 2010a. A behavioral perspective on the biophysics of the light-dependent magnetic compass: a link between directional and spatial perception? J. Exp. Biol. 213, 3247–3255. Phillips, J.B., Jorge, P.E., Muheim, R., 2010b. Light-dependent magnetic compass orientation in amphibians and insects: candidate receptors and candidate molecular mechanisms. J. R. Soc. Interface 7 (Suppl. 2), S241–S256. Phillips, J.B., Deutschlander, M.E., Freake, M.J., Borland, S.C., 2001. The role of extraocular photoreceptors in newt magnetic compass orientation: parallels between light-dependent magnetoreception and polarized light detection in vertebrates. J. Exp. Biol. 204, 2543–2552. Phillips, J.B., Freake, M.J., Fischer, J.H., Borland, C., 2002a. Behavioral titration of a magnetic map coordinate. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 188, 157–160. Phillips, J.B., Borland, S.C., Freake, M.J., Brassart, J., Kirschvink, J.L., 2002b. ‘Fixedaxis’ magnetic orientation by an amphibian: non-shoreward-directed compass orientation, misdirected homing or positioning a magnetite-based map detector in a consistent alignment relative to the magnetic field? J. Exp. Biol. 205, 3903–3914. R Development Core Team, 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Ramírez, E., Marín, G., Mpodozis, J., Letelier, J.-C., 2014. Extracellular recordings reveal absence of magneto sensitive units in the avian optic tectum. J. Comp. Physiol. A 200, 983–996. Rashid, N., Andrew, R.J., 1989. Right hemisphere advantages for topographical orientation in the domestic chick. Neuropsychologia 27, 937–948. Ritz, T., 2011. Quantum effects in biology: bird navigation. Proc. Chem. 3, 262–275. Ritz, T., Adem, S., Schulten, K., 2000. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707–718. Robins, A., Phillips, C., 2010. Lateralised visual processing in domestic cattle herds responding to novel and familiar stimuli. Laterality 15, 514–534. Rogers, L.J., Andrew, R., 2002. Comparative Vertebrate Lateralization. Cambridge University Press. Sandoval, E.L., Wajnberg, E., Esquivel, D.M., de Barros, H.L., Acosta-Avalos, D., 2012. Magnetic Orientation in Solenopsis sp. ants. J. Insect Behav. 25, 612–619. Schneider, F., 1963. Systematische Variationen in der elektrischen, magnetischen,
E.P. Malkemper et al. / Journal of Theoretical Biology 399 (2016) 141–147
und geographisch-ultraoptischen Orientierung des Maikafers. Vierteljahrsschr. der Naturforschenden Ges. Zur. 108, 373–416. Semm, P., Demaine, C., 1986. Neurophysiological properties of magnetic cells in the pigeon's visual system. J. Comp. Physiol. A: Neuroethol. Sens., Neural Behav. Physiol. 159, 619–625. Semm, P., Beason, R., 1990. Responses to small magnetic variations by the trigeminal system of the Bobolink. Brain Res. Bull. 25, 735–740. Semm, P., Nohr, D., Demaine, C., Wiltschko, W., 1984. Neural basis of the magnetic compass: interactions of visual, magnetic and vestibular inputs in the pigeon's brain. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 155, 283–288. Shimizu, T., Bowers, A.N., Budzynski, C.A., Kahn, M.C., Bingman, V.P., 2004. What does a pigeon (Columba livia) brain look like during homing? Selective examination of ZENK expression. Behav. Neurosci. 118, 845. Slaby, P., Tomanova, K., Vácha, M., 2013. Cattle on pastures do align along the North–South axis, but the alignment depends on herd density. J. Comp. Physiol. A, 1–7. Solov'yov, I.A., Mouritsen, H., Schulten, K., 2010. Acuity of a cryptochrome and vision-based magnetoreception system in birds. Biophys. J. 99, 40–49. Thalau, P., Ritz, T., Burda, H., Wegner, R.E., Wiltschko, R., 2006. The magnetic compass mechanisms of birds and rodents are based on different physical principles. J. R. Soc. Interface 3, 583–587. Treiber, C.D., Salzer, M.C., Riegler, J., Edelman, N., Sugar, C., Breuss, M., Pichler, P., Cadiou, H., Saunders, M., Lythgoe, M., Shaw, J., Keays, D.A., 2012. Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484, 367–370. Vácha, M., Kvicalova, M., Puzova, T., 2010. American cockroaches prefer four cardinal geomagnetic positions at rest. Behaviour 147, 425–440. Vargas, J.P., Siegel, J.J., Bingman, V.P., 2006. The effects of a changing ambient magnetic field on single-unit activity in the homing pigeon hippocampus. Brain
147
Res. Bull. 70, 158–164. Walker, S.F., 1980. Lateralization of functions in the vertebrate brain: a review. Br. J. Psychol. 71, 329–367. Wendt, P.E., Risberg, J., 1994. Cortical activation during visual spatial processing: Relation between hemispheric asymmetry of blood flow and performance. Brain Cogn. 24, 87–103. Wiltschko, R., Wiltschko, W., 2012. Magnetoreception, Sensing in Nature. Springer, pp. 126–141. Wiltschko, R., Stapput, K., Ritz, T., Thalau, P., Wiltschko, W., 2007. Magnetoreception in birds: different physical processes for two types of directional responses. Hum. Front. Sci. Program J. 1, 41–48. Wiltschko, W., Wiltschko, R., 1972. Magnetic compass of European robins. Science 176, 62–64. Wiltschko, W., Wiltschko, R., 2007. Magnetoreception in birds: two receptors for two different tasks. J. Ornithol. 148, S61–S76. Wiltschko, W., Munro, U., Ford, H., Wiltschko, R., 2003. Lateralisation of magnetic compass orientation in silvereyes, Zosterops lateralis. Aust. J. Zool. 51, 597–602. Wiltschko, W., Traudt, J., Güntürkün, O., Prior, H., Wiltschko, R., 2002. Lateralization of magnetic compass orientation in a migratory bird. Nature 419, 467–470. Wilzeck, C., Wiltschko, W., Güntürkün, O., Wiltschko, R., Prior, H., 2010. Lateralization of magnetic compass orientation in pigeons. J. R. Soc. Interface 7 (Suppl. 2), S235–S240. Wu, L.-Q., Dickman, J.D., 2011. Magnetoreception in an avian brain in part mediated by inner ear lagena. Curr. Biol. 21, 418–423. Wu, L.Q., Dickman, J.D., 2012. Neural correlates of a magnetic sense. Science 336, 1054. Zapka, M., Heyers, D., Hein, S., Engels, S., Schneider, N.L., Hans, J., Weiler, S., Dreyer, D., Kishkinev, D., Wild, J.M., Mouristen, H., 2009. Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461, 1274–1277.