Light-dependent magnetoreception: quantum catches and opponency mechanisms of possible photosensitive molecules

Abstract

Dozens of experiments on magnetosensitive, migratory birds have shown that their magnetic orientation behavior depends on the spectrum of light under which they are tested. However, it is not certain whether this is due to a direct effect on the magnetoreceptive system and which photosensitive molecules may be involved. We examined 62 experiments of light-dependent magnetoreception in three crepuscular and nocturnal migrants (48 for the European robin Erithacus rubecula, ten for the silvereye Zosterops lateralis, and four on the garden warbler Sylvia borin). For each experiment, we calculated the relative quantum catches of seven of the eight known photosensitive molecules found in the eyes of passerine birds: a short- (SW), medium- (MW) and long-wavelength (LW) cone pigment, rhodopsin, melanopsin, and cryptochrome in its fully-oxidized and semiquinone state. The following five opponency processes were also calculated: LW–SW, LW–MW, MW–SW, LW–(MW+SW), and cryptochrome–semiquinone. While the results do not clearly show which receptor system may be responsible for magnetoreception, it suggests several candidates that may inhibit the process. The two significant inhibitors of magnetoreceptive behavior were overall irradiances (from 400 to 700 nm) higher than those found at sunset and high quantum catch by the LW receptor. The results were also consistent with the hypothesis that high quantum catch by the semiquinone form of cryptochrome inhibits magnetoreception. The opponency mechanism that best separated oriented from non-oriented behavior was LW–MW, where a difference above a certain level inhibited orientation. Certain regions of experimental spectral space have been over-sampled, while large regions have not been sampled at all, including: (1) from 440 to 500 nm at all irradiance levels, (2) for wavelengths longer than 570 nm from 10¹² to 3×10¹² photons s^–1 cm^–2 and (3) for wavelengths less than 560 nm from 10¹² to 3×10¹² photons s^–1 cm^–2 and below 5×10¹¹ photons s^–1 cm^–2. Experiments under these conditions are needed to draw further conclusions.