Abstract
Although ferrimagnetic material appears suitable as a basis of magnetic field perception in animals, it is not known by which mechanism magnetic particles may transduce the magnetic field into a nerve signal. Provided that magnetic particles have remanence or anisotropic magnetic susceptibility, an external magnetic field will exert a torque and may physically twist them. Several models of such biological magnetic-torque transducers on the basis of magnetite have been proposed in the literature. We analyse from first principles the conditions under which they are viable. Models based on biogenic single-domain magnetite prove both effective and efficient, irrespective of whether the magnetic structure is coupled to mechanosensitive ion channels or to an indirect transduction pathway that exploits the strayfield produced by the magnetic structure at different field orientations. On the other hand, torque-detector models that are based on magnetic multi-domain particles in the vestibular organs turn out to be ineffective. Also, we provide a generic classification scheme of torque transducers in terms of axial or polar output, within which we discuss the results from behavioural experiments conducted under altered field conditions or with pulsed fields. We find that the common assertion that a magnetoreceptor based on single-domain magnetite could not form the basis for an inclination compass does not always hold.
Highlights
In the nearly 50 years since Lowenstam (1962) reported the presence of the ferromagnetic mineral magnetite (Fe3O4) as a hardening agent in the radular teeth of the Polyplacophoran molluscs, and suggested it might possibly be used as a magnetic field sensor, it has been found as a matrix-mediated biological precipitate in a plethora of living organisms, including insects (Gould et al 1978), vertebrates (Walcott et al 1979), bacteria (Frankel et al 1979) and even protists (Bazylinski et al 2000)
We show that an effective torque transducer can be realized in a regime where the magnetic torque is one order of magnitude lower than the elastic spring constants involved
If the torque mechanism is directly coupled to a mechanotransductive pathway, the rigidity of the mechanosensitive structures (equation (3.10)) is an essential part of the torque balance and will typically be of the order of 102kT/rad per connecting filament
Summary
In the nearly 50 years since Lowenstam (1962) reported the presence of the ferromagnetic mineral magnetite (Fe3O4) as a hardening agent in the radular teeth of the Polyplacophoran molluscs (the chitons), and suggested it might possibly be used as a magnetic field sensor, it has been found as a matrix-mediated biological precipitate in a plethora of living organisms, including insects (Gould et al 1978), vertebrates (Walcott et al 1979), bacteria (Frankel et al 1979) and even protists (Bazylinski et al 2000). Natural selection for size, shape, chemistry, crystallographic orientation and several other properties of biological magnetite had converged on the same solutions for producing single-domain crystals in magnetotactic bacteria (Kirschvink & Lowenstam 1979), confirming both the geophysical work and the role of the ferromagnetic materials in their magnetic response. Our focus is mainly on single-domain magnetite (§3), yet for the sake of completeness we start with a more general treatment of the physics of torque transducers
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