Resonance effects indicate a radical-pair mechanism for avian magnetic compass

Abstract

Migratory birds are known to use the geomagnetic field as a source of compass information. There are two competing hypotheses for the primary process underlying the avian magnetic compass, one involving magnetite, the other a magnetically sensitive chemical reaction. Here we show that oscillating magnetic fields disrupt the magnetic orientation behaviour of migratory birds. Robins were disoriented when exposed to a vertically aligned broadband (0.1-10 MHz) or a single-frequency (7-MHz) field in addition to the geomagnetic field. Moreover, in the 7-MHz oscillating field, this effect depended on the angle between the oscillating and the geomagnetic fields. The birds exhibited seasonally appropriate migratory orientation when the oscillating field was parallel to the geomagnetic field, but were disoriented when it was presented at a 24 degrees or 48 degrees angle. These results are consistent with a resonance effect on singlet-triplet transitions and suggest a magnetic compass based on a radical-pair mechanism.

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

“…As discussed above, the high sensitivity of the birds' magnetic compass to RF fields, found in [21,22,24] and now confirmed by us, is difficult to explain within the existing radical-pair theory. The reason is that the time needed for the RF field to change the state of an electron spin cannot be shorter than the period of rotation of the same spin in a static field of the same amplitude (assuming all the other interactions nullified).…”

“…The amplitude of the probability oscillation depends on the direction of the magnetic field as A(1 2 cos2u), where u is the angle between the magnetic field and the anisotropy axis of the 'reference' radical, and A , 1/2 is a constant depending on the details of the radical-pair formation process. A considerable difference in the singlet yield for radical pairs with different directions of the anisotropy axis with respect to the magnetic field can develop if both the lifetime of the radical pair and disorientation time of electron moments (spin relaxation time) are comparable with or longer than (2pf L ) 21 . For B ¼ 50 mT, this time amounts to 0.1 ms. With the typical radical-pair lifetimes of the order of a few microseconds, this would give a very good directional sensitivity (provided controllable orientation of the molecules in the magnetoreceptor; see discussion of this issue in [26]).…”

“…If a weak RF field with the amplitude B RF and the frequency f B is applied at the angle w to the static field B, then, even at u ¼ 0, oscillations between the singlet and triplet configurations will occur at the Rabi frequency f R ¼ 1/2g e B RF sin w. If all the characteristic times in the system were long enough, this would equalize the singlet yield for all orientations of the molecule and, therefore, disrupt the work of the radicalpair compass. 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.…”

“…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].…”