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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 information1,2. There are two competing hypotheses for the primary process underlying the avian magnetic compass, one involving magnetite3,4,5, the other a magnetically sensitive chemical reaction6,7,8. 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° or 48° angle. These results are consistent with a resonance effect on singlet–triplet transitions and suggest a magnetic compass based on a radical-pair mechanism7,8.

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Figure 1: Experimental set-up.
Figure 2: Effects of oscillating magnetic fields on magnetic orientation behaviour of European robins.

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References

  1. Wiltschko, W. & Wiltschko, R. Magnetic compass of European robins. Science 176, 62–64 (1972)

    Article  ADS  CAS  PubMed  Google Scholar 

  2. Wiltschko, R. & Wiltschko, W. Magnetic Orientation in Animals (Springer, Berlin, 1995)

    Book  Google Scholar 

  3. Kirschvink, J. & Gould, J. Biogenic magnetite as a basis for magnetic field detection in animals. BioSystems 13, 181–201 (1981)

    Article  CAS  PubMed  Google Scholar 

  4. Edmonds, D. T. A sensitive optically detected magnetic compass for animals. Proc. R. Soc. Lond. B 263, 295–298 (1996)

    Article  ADS  CAS  Google Scholar 

  5. Shcherbakov, V. P. & Winklhofer, M. The osmotic magnetometer: a new model for a magnetite-based magnetoreceptor in animals. Eur. Biophys. J. 28, 380–392 (1999)

    Article  CAS  Google Scholar 

  6. Leask, M. J. A physico-chemical mechanism for magnetic field detection by migratory birds and homing pigeons. Nature 267, 144–145 (1977)

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Schulten, K. Magnetic field effects in chemistry and biology. Festkörperprobleme (Adv. Solid State Phys.) 22, 61–83 (1982)

    Article  CAS  Google Scholar 

  8. Ritz, T., Adem, S. & Schulten, K. A photoreceptor-based model for magnetoreception in birds. Biophys. J. 78, 707–718 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. Red light disrupts magnetic orientation of migratory birds. Nature 364, 525–527 (1993)

    Article  ADS  Google Scholar 

  10. Wiltschko, W. & Wiltschko, R. Magnetic compass orientation in birds and its physiological basis. Naturwissenschaften 89, 445–452 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Wiltschko, W., Traudt, J., Güntürkün, O., Prior, H. & Wiltschko, R. Lateralization of magnetic compass orientation in a migratory bird. Nature 419, 467–470 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  12. Kobayashi, A. & Kirschvink, J. in Electromagnetic Fields: Biological Interactions and Mechanisms (ed. Blank, M.) 367–394 (American Chemical Society Books, Washington DC, 1995)

    Book  Google Scholar 

  13. Weaver, J., Vaughn, T. & Astumian, R. Biological sensing of small differences by magnetically sensitive chemical reactions. Nature 405, 707–709 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  14. Kirschvink, J. et al. in Sensory Transduction (eds Corey, D. & Roper, S.) 225–240 (Society of General Physiologists 45th Annu. Symp., Rockefeller Univ. Press, New York, 1992)

    Google Scholar 

  15. Cintolesi, F., Ritz, T., Kay, C., Timmel, C. & Hore, P. Anisotropic recombination of an immobilized photoinduced radical pair in a 50 µT magnetic field: a model avian photomagnetoreceptor. Chem. Phys. 294, 384–399 (2003)

    Article  Google Scholar 

  16. Wiltschko, W. & Wiltschko, R. The effect of yellow and blue light on magnetic compass orientation in European Robins, Erithacus rubecula. J. Comp. Physiol. A 184, 295–299 (1999)

    Article  Google Scholar 

  17. Wiltschko, W., Gesson, M. & Wiltschko, R. Magnetic compass orientation of European robins under 565 nm green light. Naturwissenschaften 88, 387–390 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  18. Canfield, J., Belford, R., Debrunner, P. & Schulten, K. A perturbation theory treatment of oscillating magnetic fields in the radical pair mechanism. Chem. Phys. 182, 1–18 (1994)

    Article  CAS  Google Scholar 

  19. Kirschvink, J. Microwave absorption by magnetite: a possible mechanism for coupling nonthermal levels of radiation to biological systems. Bioelectromagnetics 17, 187–194 (1996)

    Article  CAS  PubMed  Google Scholar 

  20. Beason, R. C. & Nichols, J. E. Magnetic orientation and magnetically sensitive material in a transequatorial migratory bird. Nature 309, 151–153 (1984)

    Article  ADS  Google Scholar 

  21. Fleissner, G. et al. Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 458, 350–360 (2003)

    Article  CAS  PubMed  Google Scholar 

  22. Beason, R. & Semm, P. Does the ophthalmic nerve carry magnetic navigational information? J. Exp. Biol. 199, 1241–1244 (1996)

    CAS  PubMed  Google Scholar 

  23. Munro, U., Munro, J. A., Phillips, J. B., Wiltschko, R. & Wiltschko, W. Evidence for a magnetite-based navigational ‘map’ in birds. Naturwissenschaften 84, 26–28 (1997)

    Article  ADS  CAS  Google Scholar 

  24. Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. Effect of a magnetic pulse on the orientation of silvereyes, Zosterops l. lateralis, during spring migration. J. Exp. Biol. 201, 3257–3261 (1998)

    PubMed  Google Scholar 

  25. Semm, P. & Beason, R. C. Responses to small magnetic variations by the trigeminal system of the bobolink. Brain Res. Bull. 25, 735–740 (1990)

    Article  CAS  PubMed  Google Scholar 

  26. Beason, R. C. & Semm, P. in Acta XX Congr. Int. Ornithol. (ed. Bell, B. D.) 1813–1819 (New Zealand Ornithol. Congr. Trust Board, Wellington, 1991)

    Google Scholar 

  27. Batschelet, E. Circular Statistics in Biology (Academic, London, 1981)

    MATH  Google Scholar 

  28. Timmel, C., Cintolesi, F., Brocklehurst, B. & Hore, P. Model calculations of magnetic field effects on the recombination reactions of radicals with anisotropic hyperfine interactions. Chem. Phys. Lett. 334, 387–395 (2001)

    Article  ADS  CAS  Google Scholar 

  29. Wiltschko, W. in Animal Migration, Navigation and Homing (eds Koenig, K. & Keeton, W.) 302–310 (Springer, Berlin, 1978)

    Book  Google Scholar 

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Acknowledgements

We thank the Deutsche Telekom AG, especially H. Küpper, T. Loppnow and B. Marx for technical assistance, and F. Galera, S. Hilmer, C. Koschella and S. Münzner for their help with conducting the experiments. J.B.P. acknowledges the National Science Foundation for financial support. Our work was supported by the Deutsche Forschungsgemeinschaft (W.W.) and the Fetzer Institute (T.R.).

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Correspondence to Thorsten Ritz.

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Ritz, T., Thalau, P., Phillips, J. et al. Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429, 177–180 (2004). https://doi.org/10.1038/nature02534

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