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.

Figure 1

Schematic of the radical-pair mechanism. Light-induced electron transfer from a donor molecule D to an acceptor molecule A creates a radical pair, that is, two molecules each with an unpaired electron spin (up and down arrows next to D and A). Singlet and triplet states, defined by the relative orientation of the electron spins, interconvert due to the combined effects of internal and external magnetic fields. Singlet and triplet radical pairs decay into singlet and triplet products respectively, with relative yields indicated by the sizes of the circles. The relative yields of singlet and triplet products depend on the orientation of the external magnetic field with respect to that of the radicals. The arrows and circles at the bottom of the diagram symbolize pathways of product formation and reaction yields for two different orientations.

Figure 2

Orientation behavior of European robins in the local geomagnetic field: effects of added 480 nT oscillating fields of various frequencies. The symbols at the periphery of the circles mark the mean headings of the test birds based on three recordings each; the arrows represent the corresponding mean vectors. For the static field, the data from different years are given by different symbols; the three mean vectors almost coincide. The two inner circles are the 5% (dotted) and 1% significance limits of the Rayleigh test (17).

Figure 3

Orientation behavior of European robins: effects of added oscillating fields of various intensities and frequencies. (Left) Responses in the local geomagnetic field. (Right) Responses in a magnetic field of doubled intensity after preexposing birds to this field for 3 h. (Top diagrams) Oriented responses in the expected migratory direction in the static fields alone. (Diagrams below) Responses with oscillating fields added. (In the geomagnetic field, there were no tests at 0.658 MHz, 48, 15, and 5 nT; at 1.315 MHz, 150 nT, and 2.63 MHz, 5 nT due to time constraints; the same applies to the 92 μT static field at 1.315 MHz, 15, and 5 nT and at 2.63 MHz, 150 nT). Oriented responses are observed if the added high-frequency fields are weak, but test birds are disoriented when the intensity of the high-frequency field crosses a threshold. The threshold depends on the intensity of the static field and the frequency of the oscillating field: 1.315 MHz fields have the most pronounced effect on orientation in the geomagnetic field, whereas 2.63 MHz fields have the most pronounced effect in an ambient field of doubled intensity. Symbols as in Fig. 2.

Figure 4

Calculated spectra of a model radical pair in magnetic fields of 46 and 92 μT. Δ_iso and Δ_an are, respectively, the isotropic and anisotropic parts of the fractional change in the reaction product yield produced by a 1 μT magnetic field oscillating at frequencies between 1 and 4 MHz. For details of the calculations, including the definitions of Δ_iso and Δ_an, see supplementary information. Strong resonances at the Larmor frequencies that correspond to the two applied magnetic field intensities are clearly seen. Much weaker resonances, arising principally from hyperfine interactions, are visible at other frequencies; the vertical scaling factors for each simulation are as indicated. The four traces are offset vertically from zero for clarity. The dots on the vertical axis show the values of Δ_iso and Δ_an for a 1 μT additional magnetic field at zero frequency.