Light-dependent magnetoreception in birds: the crucial step occurs in the dark - PubMed (original) (raw)

Light-dependent magnetoreception in birds: the crucial step occurs in the dark

Roswitha Wiltschko et al. J R Soc Interface. 2016 May.

Abstract

The Radical Pair Model proposes that the avian magnetic compass is based on spin-chemical processes: since the ratio between the two spin states singlet and triplet of radical pairs depends on their alignment in the magnetic field, it can provide information on magnetic directions. Cryptochromes, blue light-absorbing flavoproteins, with flavin adenine dinucleotide as chromophore, are suggested as molecules forming the radical pairs underlying magnetoreception. When activated by light, cryptochromes undergo a redox cycle, in the course of which radical pairs are generated during photo-reduction as well as during light-independent re-oxidation. This raised the question as to which radical pair is crucial for mediating magnetic directions. Here, we present the results from behavioural experiments with intermittent light and magnetic field pulses that clearly show that magnetoreception is possible in the dark interval, pointing to the radical pair formed during flavin re-oxidation. This differs from the mechanism considered for cryptochrome signalling the presence of light and rules out most current models of an avian magnetic compass based on the radical pair generated during photo-reduction. Using the radical pair formed during re-oxidation may represent a specific adaptation of the avian magnetic compass.

Keywords: avian magnetic compass; cryptochrome 1a; flavin redox cycle; light-activation; radical pairs.

© 2016 The Authors.

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Figures

Figure 1.

Figure 1.

Redox cycle of FAD, the chromophore of cryptochrome. The radical pairs are given in parentheses; coloured arrows, photo-reduction by the respective wavelengths (see text); black arrows, light-independent reactions of re-oxidation (after [19], modified). ‘Z’ in the radical pair generated during re-oxidation stands for a radical whose nature is not yet clear ([21] and text).

Figure 2.

Figure 2.

Orientation behaviour during the pre-test series. Above: testing the required duration of the presence of the geomagnetic field under continuous green light, with (a) the geomagnetic field present 100 ms s–1, 900 ms compensated; (b) the geomagnetic field present 300 ms s–1, 700 ms compensated. Below: testing flickering light in a constant magnetic field: tests in the geomagnetic field with light present 300 ms s–1, 700 ms total darkness. (c) Under flickering 502 nm turquoise light; (d) under flickering 565 nm green light. The schemes above the circles symbolize the distribution of light (above, green or turquoise) and magnetic field (below; brown). The triangles at the peripheries of the circles mark the mean headings of individual birds based on three recordings each, solid: unimodal, open: preferred end of an axis. The arrows represent the grand mean vectors drawn proportional to the radius of the circle, and the two inner circles mark the 5% (dotted) and the 1% significance border of the Rayleigh test [25].

Figure 3.

Figure 3.

Orientation of birds when the magnetic field and light was present alternatingly. (a) Orientation under 502 nm turquoise light when the light was on and the magnetic field compensated for ca 300 ms, then the light was off and the geomagnetic field present for ca 700 ms, then again the light was on and the magnetic field compensated, etc. (b) Orientation in the same condition under 565 nm green light. Symbols as in figure 2.

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