Magnetic compass orientation in two strictly subterranean rodents: learned or species-specific innate directional preference?

Abstract

SUMMARYEvidence for magnetoreception in mammals remains limited. Magnetic compass orientation or magnetic alignment has been conclusively demonstrated in only a handful of mammalian species. The functional properties and underlying mechanisms have been most thoroughly characterized in Ansellʼs mole-rat, Fukomys anselli, which is the species of choice due to its spontaneous drive to construct nests in the southeastern sector of a circular arena using the magnetic field azimuth as the primary orientation cue. Because of the remarkable consistency between experiments, it is generally believed that this directional preference is innate. To test the hypothesis that spontaneous southeastern directional preference is a shared, ancestral feature of all African mole-rats (Bathyergidae, Rodentia), we employed the same arena assay to study magnetic orientation in two other mole-rat species, the social giant mole-rat, Fukomys mechowii, and the solitary silvery mole-rat, Heliophobius argenteocinereus. Both species exhibited spontaneous western directional preference and deflected their directional preference according to shifts in the direction of magnetic north, clearly indicating that they were deriving directional information from the magnetic field. Because all of the experiments were performed in total darkness, our results strongly suggest that all African mole-rats use a lightindependent magnetic compass for near-space orientation. However, the spontaneous directional preference is not common and may be either innate (but species-specific) or learned. We propose an experiment that should be performed to distinguish between these two alternatives.Supplementary material available online at

Magnetic alignment in mammals and other animals

“…Magnetic orientation has been convincingly demonstrated in six rodent species using nesting in a circular arena or a radial maze as an orientation assay (Burda et al, 1990(Burda et al, , 1991Marhold et al, 1997aMarhold et al, ,b, 2000Kimchi and Terkel 2001;Deutschlander et al, 2003;Muheim et al, 2006;Oliveriusová et al, under review). The very fact that this assay is not based on any goal directed behavioral task raises the question as to whether the spontaneous drive to build nests in a certain sector of the arena/maze constitutes true compass orientation or MA.…”

“…The situation is less clear in strictly subterranean, congenitally microphthalmic mole-rats, which exhibit a spontaneous directional preference (Burda et al, 1990(Burda et al, , 1991Marhold et al, 1997aMarhold et al, ,b, 2000Kimchi and Terkel 2001;Oliveriusová et al, under review). Indeed, it has been repeatedly suggested that the magnetic orientation of mole-rats can be viewed as an expression of MA (Deutschlander et al, 2003;Muheim et al, 2006;Phillips et al, 2010).…”

Rapid Learning of Magnetic Compass Direction by C57BL/6 Mice in a 4-Armed ‘Plus’ Water Maze

“…Among mammals, bats [3,4], two families of subterranean molerats [5–7], as well as Siberian hamsters and C57BL/6 mice [8–10], have been shown to rely on magnetic cues to determine compass headings. Magnetic cues have also been implicated in the tendency of free-living mammals as diverse as cattle, deer, and foxes to preferentially align their body axes along the North–South axis [11–13].…”

“…It is noteworthy that all of the studies demonstrating the use of magnetic cues by rodents, with the exception of [14], have used assays that involve spontaneous or learned nest positioning behaviors [6,7,9,15]. Consequently, one possible explanation for the lack of evidence in other hamster and mouse studies is that rodents only utilize magnetic compass cues in certain behavioral contexts such as nest-building.…”

“…Consequently, one possible explanation for the lack of evidence in other hamster and mouse studies is that rodents only utilize magnetic compass cues in certain behavioral contexts such as nest-building. However, given the obvious utility of a global reference system provided by the Earth’s magnetic field [1,16], the failure to use magnetic cues in other spatial tasks would be surprising, all the more so because magnetic responses in molerats appear quite robust, having been demonstrated in multiple species belonging to two different families and in studies carried out by at least four different laboratories [5–7,14,17,18]. …”