Magnetic Compass of Birds Is Based on a Molecule with Optimal Directional Sensitivity

Abstract

The avian magnetic compass has been well characterized in behavioral tests: it is an "inclination compass" based on the inclination of the field lines rather than on the polarity, and its operation requires short-wavelength light. The "radical pair" model suggests that these properties reflect the use of specialized photopigments in the primary process of magnetoreception; it has recently been supported by experimental evidence indicating a role of magnetically sensitive radical-pair processes in the avian magnetic compass. In a multidisciplinary approach subjecting migratory birds to oscillating fields and using their orientation responses as a criterion for unhindered magnetoreception, we identify key features of the underlying receptor molecules. Our observation of resonance effects at specific frequencies, combined with new theoretical considerations and calculations, indicate that birds use a radical pair with special properties that is optimally designed as a receptor in a biological compass. This radical pair design might be realized by cryptochrome photoreceptors if paired with molecular oxygen as a reaction partner.

Magnetic orientation of garden warblers ( Sylvia borin ) under 1.4 MHz radiofrequency magnetic field

“…15 nT applied at the angle of 248 to the static field [22], this would mean 2 ms that exceeds the most daring estimates of electron spin relaxation time in organic radicals. Further, one must take into account that the static magnetic field varied from 46 to 47.4 mT for different experimental cages in [22], but the RF field with the amplitude B RF ! 15 nT and frequency 1.315 MHz always caused disorientation, while for most cages it was, in fact, off the resonance.…”

“…However, because now both the lifetime and spin relaxation time must be longer than (2pf R ) 21 , and f R ( f B (because B RF ( B), the criterion becomes much more severe: for the lowest RF amplitude that was reported to disrupt orientation of European robins, i.e. 15 nT applied at the angle of 248 to the static field [22], this would mean 2 ms that exceeds the most daring estimates of electron spin relaxation time in organic radicals. Further, one must take into account that the static magnetic field varied from 46 to 47.4 mT for different experimental cages in [22], but the RF field with the amplitude B RF !…”

“…To summarize this long introduction, experimental works [21,22,24] and consequent theoretical studies aimed at their explanation [25,28] have led to a dilemma: either the experiments of the Frankfurt group on the RF field effect upon orientation of European robins were flawed and their results are incorrect, or the RPM in its present form does not correctly reproduce the physics of the bird's magnetic compass. As the RPM is one of the mainstream theories of magnetoreception, and there exists a considerable body of experimental evidence supporting the idea that compass magnetoreception is based on the vision system of birds, independent experimental studies aimed at confirmation or negation of the results of previous studies [21,22,24] are of key importance for the further development of the science of magnetoreception [10].…”

“…As the RPM is one of the mainstream theories of magnetoreception, and there exists a considerable body of experimental evidence supporting the idea that compass magnetoreception is based on the vision system of birds, independent experimental studies aimed at confirmation or negation of the results of previous studies [21,22,24] are of key importance for the further development of the science of magnetoreception [10].…”

Chemical magnetoreception in birds: The radical pair mechanism

“…Bearing in mind that the periodic S 7 T interconversion induced by a Ϸ500-nT Zeeman interaction has a period of Ϸ70 s, sensitivity to such a feeble radio frequency field implies either a surprisingly long-lived spin-correlation or highly efficient signal transduction or both. In a very recent study, European robins exposed to radio frequency fields of various intensities and frequencies showed an extraordinarily sensitive response at 1.315 MHz in the local geomagnetic field (46 T), which shifted to 2.630 MHz when the birds had been preconditioned to a 92-T field (77). These resonances, at the frequency of the electron Zeeman interaction, were interpreted in terms of a radical pair in which one of the radicals was devoid of hyperfine interactions.…”