Avian magnetite-based magnetoreception: a physiologist's perspective

Abstract

It is now well established that animals use the Earth's magnetic field to perform long-distance migration and other navigational tasks. However, the transduction mechanisms that allow the conversion of magnetic field variations into an electric signal by specialized sensory cells remain largely unknown. Among the species that have been shown to sense Earth-strength magnetic fields, birds have been a model of choice since behavioural tests show that their direction-finding abilities are strongly influenced by magnetic fields. Magnetite, a ferromagnetic mineral, has been found in a wide range of organisms, from bacteria to vertebrates. In birds, both superparamagnetic (SPM) and single-domain magnetite have been found to be associated with the trigeminal nerve. Electrophysiological recordings from cells in the trigeminal ganglion have shown an increase in action potential firing in response to magnetic field changes. More recently, histological evidence has demonstrated the presence of SPM magnetite in the subcutis of the pigeon's upper beak. The aims of the present review are to review the evidence for a magnetite-based mechanism in birds and to introduce physiological concepts in order to refine the proposed models.

Figure 1.

Presence of SPM magnetite in the upper skin of the beak of the homing pigeon (Columbia livia). (a) Prussian blue staining showing iron deposits (yellow arrows) between fat cells. Scale bar: 50 µm. (b) View of the beak showing where magnetite was found by the Fleissner group. Three pairs of spots were found with different alignments. The caudal nerve terminals were mostly aligned in a longitudinal pattern, whereas the median ones where set transversally. The frontal magnetite-containing endings were aligned vertically. Scale bar: 0.5 cm. (c) Three-dimensional reconstruction of a nerve ending showing the SPM magnetite clusters (MC) connected by iron platelets (Pt). Note the presence of a giant vacuole (V) on the left of the panel. (d) Close-up diagram of magnetite clusters. Note that the cluster (SPM) is connected to the plasma membrane (PM) through filaments (B). The cluster is resting in a fibrous basket (C) and is connected to the iron platelets (D). Illustrations are taken from Fleissner et al. (2007).

Figure 2.

Trigeminal magnetosensation in birds. (a) Schematic representation of a bird head with the trigeminal system. 1, Site for the SPM magnetite found by the Fleissner group (figure 1); 2, site for iron accumulation found by Williams & Wild (2001) linked to trigeminal nerve ending in the pigeon (Columbia livia) and in the zebrafinch (Taeniopygia guttata); 3, electrophysiological recording from the trigeminal nerve in the bobolink by Beason & Semm (1987); 4, electrophysiological recordings from trigeminal neurons by Semm & Beason (1990) in the bobolink; TG, trigeminal ganglion; C, cere; V1, ophthalmic branch of trigeminal nerve; V2, maxillary branch; V3, mandibular branch. Figure modified from Fleissner et al. (2003). (b) Extracellular recordings obtained from cells within the trigeminal ganglion of the bobolink showing an increased activity in the presence of a magnetic stimulus (solid bar), which shows a decrease in the vertical component of the GMF. Note that these are three successive responses and that they decrease in frequency. Horizontal scale bar 1 s, vertical 2 mV. (c) Stimulus-response curve obtained with the same conditions as in (b). (d) Application of a strong magnet close to the preparation triggers the same response as described in (b). Scale bar: horizontal 50 ms, vertical 2 mV. (b–d) are taken from Semm & Beason (1990) with permission of Elsevier.

Figure 3.

Proposed scenarios for mechanically based magnetoreception. (a) Mechanosensitive ion channels are located in the membrane but do not have a physical link with the magnetite. Magnetite field changes (ΔB) trigger movement of a SPM magnetite cluster or a chain of clusters (right panel), which in turn induces deformation in the plasma membrane. This latter event induces the opening of a non-selective mechanosensitive ion channel. (b) Magnetite is physically connected to the ion channel. At rest, the ion channel is blocked. Change in the magnetite field (ΔB) relieves the blockade allowing sodium and calcium entry into the cells. (c) Magnetite movement releases a second messenger (X), either directly or through the creation of tension in the membrane. The messenger binds to the ion channel and opens it. (d) Mechanism based on auditory hair cell mechanotransduction. In this model, a cell containing magnetite is linked to a neighbouring nerve terminal through a ‘tip link’ (blue filament). The ion channel is linked via a molecular motor (Myo) to actin filaments (red). Movements in the magnetite-containing compartment stretch the link and open the ion channel. After channel opening, a molecular motor could reposition the ion channel reducing the tension in the link and allowing the system to be stimulated again (step 3).