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

Abstract

Summary In terrestrial organisms, sensitivity to the Earth's magnetic field is mediated by at least two different magnetoreception mechanisms, one involving biogenic ferromagnetic crystals (magnetite/maghemite) and the second involving a photo-induced biochemical reaction that forms long-lasting, spin-coordinated, radical pair intermediates. In some vertebrate groups (amphibians and birds), both mechanisms are present; a light-dependent mechanism provides a directional sense or ‘compass’, and a non-light-dependent mechanism underlies a geographical-position sense or ‘map’. Evidence that both magnetite- and radical pair-based mechanisms are present in the same organisms raises a number of interesting questions. Why has natural selection produced magnetic sensors utilizing two distinct biophysical mechanisms? And, in particular, why has natural selection produced a compass mechanism based on a light-dependent radical pair mechanism (RPM) when a magnetite-based receptor is well suited to perform this function? Answers to these questions depend, to a large degree, on how the properties of the RPM, viewed from a neuroethological rather than a biophysical perspective, differ from those of a magnetite-based magnetic compass. The RPM is expected to produce a light-dependent, 3-D pattern of response that is axially symmetrical and, in some groups of animals, may be perceived as a pattern of light intensity and/or color superimposed on the visual surroundings. We suggest that the light-dependent magnetic compass may serve not only as a source of directional information but also provide a spherical coordinate system that helps to interface metrics of distance, direction and spatial position.

Magnetic compass orientation in two strictly subterranean rodents: learned or species-specific innate directional preference?

“…As noted above, a lightindependent, magnetite-based compass has also been reported in microphthalmic echolocating bats (Wang et al, 2007;Holland et al, 2008). By contrast, recent evidence suggests that the magnetic compass of epigeic rodents such as the Siberian hamster, Phodopus sungorus, and C57BL/6J mice has more in common with birds than with mole rats; most notably it seems to be disrupted by low-level fields oscillating in the MHz range (Phillips et al, 2010) Phillips, unpublished). These findings point to an intriguing possibility that two fundamentally different mechanisms, namely a light-independent, magnetite-based mechanism (for reviews, see Kirschvink et al, 2001;Winklhofer and Kirschvink, 2010) and a light-induced, photoreceptor-based mechanism (Ritz et al, 2000), underlie magnetic compass orientation in rodents.…”

Homing in rocky intertidal fish. Are Lipophrys pholis L. able to perform true navigation?

“…True navigation implies that animals orient themselves by relying on cues available at the unfamiliar release site, and these usually are cues with a worldwide geographic distribution such as magnetic cues (Wiltschko and Wiltschko 1995;Lohmann 1991), lightdependent cues (Muheim et al 2006;Phillips et al 2010), infrasound cues (Hagstrum 2000), or odor cues (Jorge 2011;Wallraff 2005). In Experiment 3, we showed that adult L. pholis were able to orient themselves toward their home areas even if they were placed in an unfamiliar distant area, and they did so by relying on cues available in the unfamiliar area (Fig.…”

Behavioural and physiological mechanisms of polarized light sensitivity in birds

“…According to current theory, birds may perceive the magnetic field as a three-dimensional pattern superimposed on their visual field (e.g. [80,81,86]). If PL reception takes place in parallel to magnetoreception, we would therefore expect an equally high resolution also for this system.…”