Naturwissenschaften (2014) 101:557–563 DOI 10.1007/s00114-014-1192-0
ORIGINAL PAPER
Spontaneous expression of magnetic compass orientation in an epigeic rodent: the bank vole, Clethrionomys glareolus Ludmila Oliveriusová & Pavel Němec & Zuzana Pavelková & František Sedláček
Received: 9 January 2014 / Revised: 23 April 2014 / Accepted: 23 May 2014 / Published online: 10 June 2014 # Springer-Verlag Berlin Heidelberg 2014
Abstract Magnetoreception has been convincingly demonstrated in only a few mammalian species. Among rodents, magnetic compass orientation has been documented in four species of subterranean mole rats and two epigeic (i.e. active above ground) species—the Siberian hamster and the C57BL/ 6J mouse. The mole rats use the magnetic field azimuth to determine compass heading; their directional preference is spontaneous and unimodal, and their magnetic compass is magnetite-mediated. By contrast, the primary component of orientation response is learned in the hamster and the mouse, but both species also exhibit a weak spontaneous bimodal preference in the natural magnetic field. To determine whether the magnetic compass of wild epigeic rodents features the same functional properties as that of laboratory rodents, we investigated magnetic compass orientation in the bank vole Clethrionomys glareolus (Cricetidae, Rodentia). The voles exhibited a robust spontaneous bimodal directional preference, i.e. built nests and slept preferentially along the northsouth axis, and deflected their directional preference according to a shift in the direction of magnetic north, clearly indicating that they were deriving directional information from the magnetic field. Thus, bimodal, axially symmetrical directional choice seems to be a common feature shared by Communicated by: Sven Thatje Electronic supplementary material The online version of this article (doi:10.1007/s00114-014-1192-0) contains supplementary material, which is available to authorized users. L. Oliveriusová (*) : F. Sedláček Department of Zoology, Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic e-mail:
[email protected] P. Němec : Z. Pavelková Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, 128 44 Praha 2, Czech Republic
epigeic rodents. However, spontaneous directional preference in the bank vole appeared to be more pronounced than that reported in the hamster and the mouse. These findings suggest that bank voles are well suited for future studies investigating the adaptive significance and mechanisms of magnetic orientation in epigeic rodents. Keywords Spatial orientation . Magnetoreception . Magnetite-based mechanism . Radical pair-basedmechanism . Bank vole
Introduction Diverse animals, including representatives of all five vertebrate classes, use the Earth’s magnetic field as a cue for orientation (Wiltschko and Wiltschko 1995, 2005). However, the evidence for magnetoreception in mammals remains limited. Magnetic compass orientation has been convincingly demonstrated in four species of subterranean rodents (Burda et al. 1990; Kimchi and Terkel 2001; Oliveriusová et al. 2012), two epigeic rodents (Deutschlander et al. 2003; Muheim et al. 2006; Phillips et al. 2013) and three species of bats (Holland et al. 2006, 2010; Wang et al. 2007). In addition, spontaneous magnetic alignment (a fixed directional response that is not directed towards a specific goal) in grazing and resting cattle and deer as well as in hunting foxes and urinating/defecating dogs (Begall et al. 2008, 2011; Burda et al. 2009; Červený et al. 2011; Slabý et al. 2013; Hart et al. 2013; for review, see Begall et al. 2013), and behavioral reaction to extremely low-frequency electromagnetic fields in cattle and mice (Burda et al. 2009; Prato et al. 2013). Subterranean rodents, in particular the African mole rats (Bathyergidae), have become a mammalian model to study the mechanisms of magnetic compass orientation (Marhold et al. 1997a, b; Němec et al. 2001; Thalau et al. 2006; Wegner et al. 2006; Burger et al. 2010). The fact that
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the mole rat magnetic compass is light-independent, polaritybased, insensitive to magnetic fields oscillating in the megahertz range, but altered by a brief magnetic pulse that remagnetizes ferrimagnetic materials (Marhold et al. 1997a, b; Thalau et al. 2006), strongly suggesting that mole rats possess a magnetite-mediated compass. However, congenitally microphthalmic mole rats inhabiting an aphotic underground ecotope represent an extreme case of sensory adaptation (for review, see Němec et al. 2007). Therefore, it remains unclear whether the functional properties of the magnetic compass in mole rats can be generalized to other mammals. The development of an assay that would make it possible to study magnetoreception mechanisms in epigeic rodents, i.e. in traditional biological vertebrate models, has proven difficult. Early attempts to demonstrate magnetic compass orientation in epigeic rodents produced negative, ambiguous or irreproducible results (Mather and Baker 1981; Sauvé 1985; Madden and Phillips 1987; August et al. 1989). Nevertheless, the discovery that a preferred magnetic direction is learned rather than innate in the Siberian hamster (Deutschlander et al. 2003) has led to the introduction of novel experimental paradigms. Experiments involving association of magnetic field direction with either a light gradient or the position of a submerged platform in a fourarm water maze yielded unequivocal evidence for learned magnetic compass in the C57BL/6J mouse (Muheim et al. 2006; Phillips et al. 2013). Interestingly, hamsters exhibited a spontaneous bimodal preference in the natural magnetic field, but were disoriented in shifted fields with magnetic north at geographic east, south or west (Deutschlander et al. 2003). Mice showed a strong unimodal orientation relative to the magnetic direction they had been trained for, but also a weak bimodal orientation relative to magnetic north (cf. Muheim et al. 2006, Fig. 4a, b). It remains unclear whether the latter represents a residual spontaneous directional preference or a reflection of the fact that mice trained in a light gradient aligned with the north-south axis, as opposed to the east-west axis, were better oriented (for further discussion, see Painter et al. 2013). Nevertheless, since the laboratory strains used in these experiments might hypothetically rely on magnetic cues to a lesser degree than wild rodents, it remains unknown whether the axially symmetrical (i.e., polarity-independent) and weakly expressed spontaneous directional preference represents a common feature shared by all epigeic rodents. In this study, we investigated magnetic compass orientation in a wild caught rodent, the bank vole Clethrionomys glareolus (Cricetidae, Rodentia), to determine whether the magnetic compass of wild epigeic rodents exhibits the same functional properties as those found in hamster and mouse. Thereby, we tested the hypothesis that the functional characteristics and possibly also the biophysical mechanism underlying the magnetic compass differ between epigeic and subterranean rodents.
Naturwissenschaften (2014) 101:557–563
Materials and methods Animals The bank vole, C. glareolus (Schreber 1780), is a small rodent that is widely distributed in Europe between the British Isles and northern Spain in the west and central Siberia in the east. It is abundant in a wide variety of woodland habitats, and because it is easy to trap and breed, it constitutes an excellent model for laboratory studies. A total of 20 bank voles of both sexes caught in the vicinity of Ceske Budejovice (Czech Republic) were used in this study. The animals were kept individually in plastic boxes (55×35×20 cm) at the temperature of 18±1 °C and under a 12L/12D light regime at the University of South Bohemia. They were fed with rodent pellets and carrot ad libitum and provided with bedding (wood shavings) and nest material (hay). All experiments were approved by the Institutional Animal Care and Use Committee at the University of South Bohemia, and the Ministry of Education, Youth and Sports of the Czech Republic (No. 7946/2010-30). Behavioural assay The nest building assay designed to test magnetic compass orientation in mole rats (Burda et al. 1990) was followed with minor modifications. Briefly, individual bank voles were released in a circular arena (82 cm in diameter and 41 cm in height; made of opaque plastic) placed inside a four-element cube surface coil (Merritt et al. 1983). The arena was filled with a thin layer of hay as nest material and randomly distributed pieces of carrot as food. Animals were allowed to explore the arena and build a nest there overnight; tests began 1 h before the beginning of the dark phase of their light cycle and ended the following morning. The nest position or, in individuals that did not build any nest, the resting position was taken as a proxy for assessing spontaneous directional preference. Video surveillance was used to monitor the nest and resting positions. The first five minutes of each experimental hour were automatically recorded by an overhead infrared-sensitive CCD video camera equipped with an infrared diode. Between trials, the hay and food pieces were removed from the arena and discarded, and the arena was thoroughly cleaned with 1 % Triton detergent and subsequently with 70 % ethanol. Magnetic and light conditions The bank voles were tested in two different magnetic fields: the natural magnetic field (mN=0°) and a shifted field with magnetic north at geographic east (mN=90°). The total intensity (~47 μT) and the inclination (+66°) remained unchanged. The shifted field was generated by a three-axis, double-
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wrapped coil system (four 200×200-cm square coils per axis with a coil spacing of 74.4/51.2/74.4 cm and coil winding ratio of 26:11:11:26; see Merritt et al. 1983). The arena was placed in the centre of the coil system during experiments; the heterogeneities within the arena were
