Light-dependent magnetic compass in Iberian green frog tadpoles

Abstract

Here, we provide evidence for a wavelength-dependent effect of light on magnetic compass orientation in Pelophylax perezi (order Anura), similar to that observed in Rana catesbeiana (order Anura) and Notophthalmus viridescens (order Urodela), and confirm for the first time in an anuran amphibian that a 90° shift in the direction of magnetic compass orientation under long-wavelength light (≥ 500 nm) is due to a direct effect of light on the underlying magnetoreception mechanism. Although magnetic compass orientation in other animals (e.g., birds and some insects) has been shown to be influenced by the wavelength and/or intensity of light, these two amphibian orders are the only taxa for which there is direct evidence that the magnetic compass is light-dependent. The remarkable similarities in the light-dependent magnetic compasses of anurans and urodeles, which have evolved as separate clades for at least 250 million years, suggest that the light-dependent magnetoreception mechanism is likely to have evolved in the common ancestor of the Lissamphibia (Early Permian, ~294 million years) and, possibly, much earlier. Also, we discuss a number of similarities between the functional properties of the light-dependent magnetic compass in amphibians and blue light-dependent responses to magnetic stimuli in Drosophila melanogaster, which suggest that the wavelength-dependent 90° shift in amphibians may be due to light activation of different redox forms of a cryptochrome photopigment. Finally, we relate these findings to earlier studies showing that the pineal organ of newts is the site of the light-dependent magnetic compass and recent neurophysiological evidence showing magnetic field sensitivity in the frog frontal organ (an outgrowth of the pineal).

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 …”

Zebra finches have a light-dependent magnetic compass similar to migratory birds

“…Insects and amphibians trained and tested under wavelengths of light shorter than 450 nm displayed oriented behaviour towards a trained magnetic compass direction, but shifted their orientation by ∼90 deg when tested under longer wavelengths (Phillips and Borland, 1992a,b;Phillips and Sayeed, 1993;Vacha, 2004;Dommer et al, 2008;Diego-Rasilla et al, 2010. Young, inexperienced homing pigeons (Columba livia) were unable to orient towards home when transported to the release site in complete darkness or under red light (650 nm), but were well oriented when transported under green (565 nm) or full-spectrum light Wiltschko, 1981, 1998).…”

High levels of maternally transferred mercury disrupt magnetic responses of snapping turtle hatchlings (Chelydra serpentina)

“…Magnetoreception can be involved in many aspects of spatial behaviour: as a compass for local and long-distance movements (Wiltschko and Wiltschko, 1972;Landler et al, 2015;Phillips et al, 2013;Diego-Rasilla et al, 2010;Dommer et al, 2008;Freake et al, 2002) as a source of geographic position information (i.e., a magnetic map Phillips, 1986;Philips et al, 1995;Deutschlander et al, 2012) as a reference that reduces errors in path integration (Kimchi et al, 2004;Philips et al, 2010) and potentially as a spherical coordinate system that helps to encode the organism's immediate surrounding and to incorporate local landmark arrays into a global map of familiar space (Landler et al, 2015;Phillips et al, 2010). Consequently, loss of a magnetic sense could impact both long-distance movements (e.g.…”