Light‐Dependent Shift in Bullfrog Tadpole Magnetic Compass Orientation: Evidence for a Common Magnetoreception Mechanism in Anuran and Urodele Amphibians

Abstract

Previous studies have demonstrated the presence of a light-dependent magnetic compass in a urodele amphibian, the eastern red-spotted newt Notophthalmus viridescens, mediated by extraocular photoreceptors located in or near the pineal organ. Newts tested under long-wavelength ( ‡500 nm) light exhibited a 90°shift in the direction of orientation relative to newts tested under full spectrum (white) or short-wavelength light. Here we report that bullfrog tadpoles Rana catesbeiana (an anuran amphibian) exhibit a 90°shift in the direction of magnetic compass orientation under long-wavelength ( ‡500 nm) light similar to that observed in newts, suggesting that a common light-dependent mechanism mediates these responses. These findings suggest that a lightdependent magnetic compass may have been the ancestral state in this group of vertebrates.Correspondence: Michael J. Freake,

A behavioral perspective on the biophysics of the light-dependent magnetic compass: a link between directional and spatial perception?

“…To better see the correspondence, rotate and/or invert firing fields so black geometric shape matches the corresponding shape in the center of B; see Sharp (Sharp, 2002;Sharp, 2006) for additional recordings from subicular place cells with similar spatial firing fields. (D)Inverse or complementary patterns to those shown in C, which are predicted to occur if subicular place cells receive input from a LDMC mechanism with antagonistic spectral properties similar to those found in amphibians and insects (Phillips and Borland, 1992a;Phillips and Sayeed, 1993;Phillips et al, 2001;Phillips et al, 2010;Freake and Phillips, 2005;Vacha et al, 2008b).…”

“…Evidence for a RPM-based magnetic compass in some animals includes: (1) sensitivity to the axis, but not polarity, of the magnetic field ( Fig.1) (Wiltschko and Wiltschko, 1972;Phillips, 1986); (2) involvement of a light-dependent magnetoreception mechanism (Phillips and Borland, 1992a;Phillips and Borland, 1992b;Phillips and Sayeed, 1993;Freake and Phillips, 2005;Wiltschko and Wiltschko, 2005;Vacha et al, 2008b); (3) disruption of magnetic compass orientation outside a narrow window of static field intensities ; (4) the absence of an effect of 'pulse remagnetization' (Beason and Semm, 1996;Munro et al, 1997a;Munro et al, 1997b); and (5) disruption by low-level alternating fields (~0.1% of the static field strength) in the low RF range (<100MHz) that should alter the magnetic field-dependent populations of singlet and triplet energy states in a RPM (Ritz et al, 2004;Ritz et al, 2009;Henbest et al, 2004;Thalau et al, 2005;Vacha et al, 2009). In migratory birds, the effects of low-level RF fields have been shown to depend on both the intensity and relative alignment of the static magnetic field (Ritz et al, 2004;Ritz et al, 2009) .…”

“…photoreceptors, the LDMC in insects (Phillips and Sayeed, 1993;Vacha et al, 2008b), amphibians (Phillips and Borland 1992a;Deutschlander et al, 1999a;Freake and Phillips, 2005) and, possibly, birds (Muheim et al, 2002;Wiltschko et al, 2010) share functional properties (i.e. light-dependent 90deg rotations in the direction of magnetic compass orientation) that appear to result, at least in part, from an antagonistic interaction of short-and longwavelength inputs (Phillips and Borland, 1992a;Deutschlander et al, 1999b;Phillips et al, 2010).…”

Spontaneous magnetic orientation in larval Drosophila shares properties with learned magnetic compass responses in adult flies and mice.

“…When trained under the same short-wavelength light and tested under blue-green light (500nm), beetles shifted their orientation 90deg clockwise relative to the trained magnetic direction (Vácha et al, 2008). While the wavelength-dependent effects of light on magnetic compass orientation in flies and beetles could result from a change in the behavioral response rather than a change in the directional input used to guide behavior, similar wavelength-dependent 90deg shifts in magnetic compass orientation in both anuran and urodele amphibians have been shown to result from a direct effect of light on the underlying magnetoreception mechanism (Phillips and Borland, 1992;Freake and Phillips, 2005;Diego-Rasilla et al, 2010). Furthermore, preliminary evidence for photoreceptors sensitive to the alignment of an earth-strength magnetic field has been obtained in neurophysiological recordings from the frontal organ (an The Journal of Experimental Biology 216 (7) Topographic Magnetic 4ϫ …”

Magnetic compass orientation in C57BL/6J mice

“…In mole rats, the magnetic compass appears to be mediated by a mechanism involving permanently magnetic material, presumed to be particles of biogenic magnetite (Kimchi & Terkel, 2001;Marhold, Burda, Kreilos, & Wiltschko, 1997;. In contrast, the magnetic compass of songbirds and amphibians is light dependent (Deutschlander, Borland, & Phillips, 1999;Freake & Phillips, 2005;Phillips & Borland, 1992;W. Wiltschko & R. Wiltschko, 2005) and sensitive to low-level radio frequency fields (Phillips & Freake, 2006;Ritz et al, 2004), consistent with a magnetoreception mechanism involving a light-sensitive biochemical reaction (Ritz et al, 2000).…”