Migratory orientation in birds involves an inclination compass based on radical-pair processes. Under certain light regimes, however, “fixed-direction” responses are observed that do not undergo the seasonal change between spring and autumn typical for migratory orientation. To identify the underlying transduction mechanisms, we analyzed a fixed-direction response under a combination of 502 nm turquoise and 590 nm yellow light, with migratory orientation under 565 nm green light serving as the control. High-frequency fields, diagnostic for a radical-pair mechanism, disrupted migratory orientation without affecting fixed-direction responses. Local anaesthesia of the upper beak where magnetite is found in birds, in contrast, disrupted the fixed-direction response without affecting migratory orientation. The two types of responses are thus based on different physical principles, with the compass response based on a radical pair mechanism and the fixed-direction responses probably originating in magnetite-based receptors in the upper beak. Directional input from these receptors seems to affect the behavior only when the regular inclination compass does not work properly. Evolutionary considerations suggest that magnetite-based receptors may represent an ancient mechanism that, in birds, has been replaced by the modern inclination compass based on radical-pair processes now used for directional orientation.
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Abstract
RESULTS
DISCUSSION
MATERIAL AND METHODS
References
Many animals use information from the geomagnetic field for orientation and navigation (R. Wiltschko and Wiltschko, 1995; W. Wiltschko and Wiltschko, 2005). For the reception mechanisms providing this information, two models are discussed. The “radical-pair model” proposes magnetoreception by light-induced processes in specialized photopigments (Schulten, 1982; Ritz et al., 2000). The geomagnetic field can affect electron-transfer reactions of photopigments with radical-pair intermediates, and the model suggests that this sensitivity provides the basis for the ability of birds to obtain directional information from the geomagnetic field. Magnetoreception would take place in the eye; the effect of magnetic fields would modulate photoreceptor signaling and could manifest itself by forming direction-dependent activation patterns (Ritz et al., 2000; Wang et al., 2006).
The alternative model assumes magnetoreception based on magnetite, a special form of iron oxide that is rather widespread among animals (e.g., Yorke, 1979; Kirschvink and Gould, 1981; Kirschvink et al., 1985; Davila et al., 2003). In birds, remanence measurements indicated single domain magnetite particles in the heads of various species (Walcott et al., 1979; Presti and Pettigrew, 1980; Edwards et al., 1992), with concentrations in the ethmoid region (Beason and Brennan, 1986). Histological studies also showed iron-rich particles in the ethmoid region of passerine birds and pigeons (Beason and Nichols, 1984; Williams and Wild, 2001). Crystallographic methods identified clusters of smaller superparamagnetic particles within specific structures in the skin of the upper beak of pigeons (Hanzlik et al., 2000; Winklhofer et al., 2001), with subsequent histological studies revealing that they are associated with a series of small iron-based platelets all embedded within sensory nerve terminals of the ophthalmic nerve (Fleissner et al., 2003).
Other Sections▼
Abstract
RESULTS
DISCUSSION
MATERIAL AND METHODS
References
Many animals use information from the geomagnetic field for orientation and navigation (R. Wiltschko and Wiltschko, 1995; W. Wiltschko and Wiltschko, 2005). For the reception mechanisms providing this information, two models are discussed. The “radical-pair model” proposes magnetoreception by light-induced processes in specialized photopigments (Schulten, 1982; Ritz et al., 2000). The geomagnetic field can affect electron-transfer reactions of photopigments with radical-pair intermediates, and the model suggests that this sensitivity provides the basis for the ability of birds to obtain directional information from the geomagnetic field. Magnetoreception would take place in the eye; the effect of magnetic fields would modulate photoreceptor signaling and could manifest itself by forming direction-dependent activation patterns (Ritz et al., 2000; Wang et al., 2006).
The alternative model assumes magnetoreception based on magnetite, a special form of iron oxide that is rather widespread among animals (e.g., Yorke, 1979; Kirschvink and Gould, 1981; Kirschvink et al., 1985; Davila et al., 2003). In birds, remanence measurements indicated single domain magnetite particles in the heads of various species (Walcott et al., 1979; Presti and Pettigrew, 1980; Edwards et al., 1992), with concentrations in the ethmoid region (Beason and Brennan, 1986). Histological studies also showed iron-rich particles in the ethmoid region of passerine birds and pigeons (Beason and Nichols, 1984; Williams and Wild, 2001). Crystallographic methods identified clusters of smaller superparamagnetic particles within specific structures in the skin of the upper beak of pigeons (Hanzlik et al., 2000; Winklhofer et al., 2001), with subsequent histological studies revealing that they are associated with a series of small iron-based platelets all embedded within sensory nerve terminals of the ophthalmic nerve (Fleissner et al., 2003).
