Magnetic compass of birds is based on a molecule with optimal directional sensitivity

Biophysical Journal

Volumn 96, Issue 8, 2009, Pages 3451-3457

  Ritz, Thorsten ^a   Wiltschko, Roswitha ^b   Hore, P J ^c   Rodgers, Christopher T ^c   Stapput, Katrin ^b,d   Thalau, Peter ^b   Timmel, Christiane R ^c   Wiltschko, Wolfgang ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME; OXYGEN;

ARTICLE; BIRD; CALCULATION; FOWL; LIGHT; MAGNETIC FIELD; MAGNETISM; MODEL; NONHUMAN; OSCILLATION; PHOTORECEPTOR; THEORETICAL STUDY; ANIMAL; FLYING; ORIENTATION; PHYSIOLOGY; POPULATION MIGRATION; PSYCHOMOTOR PERFORMANCE; SONGBIRD;

AVES;

ANIMAL MIGRATION; ANIMALS; FLIGHT, ANIMAL; MAGNETICS; ORIENTATION; PSYCHOMOTOR PERFORMANCE; SONGBIRDS;

EID: 67649396448     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.11.072     Document Type: Article

References (57)

1. Wiltschko, W., and R. Wiltschko. 2005. Magnetic orientation and magnetoreception in birds and other animals. J. Comp. Physiol. [A]. 191:675-693.
2. Wiltschko, W. 1968. The influence of static magnetic fields on the migratory orientation of European robins (Erithacus rubecula). Z. Tierpsychol. 25:537-558.
3. Wiltschko, W., and R. Wiltschko. 1972. Magnetic compass of European robins. Science. 176:62-64.
4. Wiltschko, W., and R. Wiltschko. 2001. Light-dependent magnetore-ception in birds: the behaviour of European robins, Erithacus rubecula, under monochromatic light of various wavelengths and intensities. J. Exp. Biol. 204:3295-3302.
5. Muheim, R., J. Bäckman, and S. Åkesson. 2002. Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light. J. Exp. Biol. 205:3845-3856.
6. Wiltschko, R., K. Stapput, H. J. Bischof, and W. Wiltschko. 2007. Light-dependent magnetoreception in birds: increasing intensity of monochromatic light changes the nature of the response. Front. Zool. 4(5). doi: 10.1186/1742-994-4-5.
7. Ritz, T., S. Adem, and K. Schulten. 2000. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78:707-718.
8. Wang, K., E. Mattern, and T. Ritz. 2006. On the use of magnets to disrupt the physiological compass of birds. Phys. Biol. 3:220-231.
9. Timmel, C. R., U. Till, B. Brocklehurst, K. A. McLauchlan, and P. J. Hore. 1998. Effects of weak magnetic fields on free radical recombination reactions. Mol. Phys. 95:71-89.
10. Wiltschko, W., J. Traudt, O. Güntürkün, H. Prior, and R. Wiltschko. 2002. Lateralisation of magnetic compass orientation in a migratory bird. Nature. 419:467-470.
11. Maeda, K., K. B. Henbest, F. Cintolesi, I. Kuprov, C. T. Rodgers, et al. 2008. Chemical compass model of avian magnetoreception. Nature. 453:387-390.
12. Weaver, J., T. E. Vaughan, and R. D. Astumian. 2000. Biological sensing of small field differences by magnetically sensitive chemical reactions. Nature. 405:707-709.
13. Henbest, K. B., P. Kukura, C. T. Rodgers, P. J. Hore, and C. R. Timmel. 2004. Radiofrequency magnetic field effects on a radical recombination reaction: a diagnostic test for the radical pair mechanism. J. Am. Chem. Soc. 126:8102-8103.
14. Weil, J. A., and J. R. Bolton. 2007. Electron Paramagnetic Resonance: Elementary Theory and Practical Applications, 2nd edition. Wiley & Sons, New York, NY.
15. Ritz, T., P. Thalau, J. B. Phillips, R. Wiltschko, and W. Wiltschko. 2004. Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature. 429:177-180.
16. Thalau, P., T. Ritz, K. Stapput, R. Wiltschko, and W. Wiltschko. 2005. Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften. 92:86-90.
17. Wiltschko, W., K. Stapput, P. Thalau, and R. Wiltschko. 2006. Avian magnetic compass: fast adjustment to intensities outside the functional window. Naturwissenschaften. 93:300-304.
18. Batschelet, E. 1981. Circular Statistics in Biology. Academic Press, London.
19. Rodgers, C. T., S. A. Norman, K. B. Henbest, C. R. Timmel, and P. J. Hore. 2007. Determination of radical re-encounter probability distributions from magnetic field effects on reaction yields. J. Am. Chem. Soc. 129:6746-6755.
20. Efimova, O., and P. J. Hore. 2008. The role of exchange and dipolar interactions in the radical pair model of the avian magnetic compass. Biophys. J. 94:1565-1574.
21. Cintolesi, F., T. Ritz, C. W. M. Kay, C. R. Timmel, and P. J. Hore. 2003. Anisotropic recombination of an immobilized photoinduced radical pair in a 50-mT magnetic field: a model avian photomagnetore-ceptor. Chem. Phys. 294:385-399.
22. Möller, A., W. Sagasser, W. Wiltschko, and B. Schierwater. 2004. Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass. Naturwissenschaften. 91:585-588.
23. Mouritsen, H., U. Janssen-Bienhold, M. Liedvogel, G. Feenders, J. Stalleicken, et al. 2004. Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proc. Natl. Acad. Sci. USA. 101:14294-14299.
24. Liedvogel, M., M. Maeda, K. Henbest, E. Schleicher, T. Simon, et al. 2007. Chemical magnetoreception: bird cryptochrome 1a is excited by blue light and forms long-lived radical-pairs. PLoS ONE. 2(10):e1106. doi: 10.1371/journal.pone.0001106.
25. Gegear, R. J., A. Casselman, S. Waddell, and S. M. Reppert. 2008. Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature. 454:1014-1018.
26. Ahmad, M., and A. R. Cashmore. 1993. HY4 gene of Arabidopsis thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature. 366:162-166.
27. Sancar, A. 2003. Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103:2203-2237.
28. Haque, R., S. S. Charausia, J. H. Wessel, and P. M. Iuvone. 2002. Dual regulation of cryptochrome I mRNA expression in chicken retina by light and circadian oscillators. Neuroreport. 13:2247-2251.
29. Giovani, B., M. Byrdin, M. Ahmad, and K. Brettel. 2003. Light-induced electron transfer in a cryptochrome blue-light photoreceptor. Nat. Struct. Biol. 6:489-490.
30. Bouly, J. P., E. Schleicher, M. Dionisio-Sese, F. Vandenbussche, D. Van Der Straeten, et al. 2007. Cryptochrome blue light photoreceptors are activated through interconversion of flavin redox states. J. Biol. Chem. 282:9383-9391.
31. Ahmad, M., P. Galland, T. Ritz, R. Wiltschko, and W. Wiltschko. 2007. Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana. Planta. 225:615-624.
32. Solov'yov, I. A., D. E. Chandler, and K. Schulten. 2007. Magnetic field effects in Arabidopsis thaliana cryptochrome-1. Biophys. J. 92:2711-2726.
33. Henbest, K. B., K. Maeda, P. J. Hore, M. Joshi, A. Bacher, et al. 2008. Magnetic field effect on the photoactivation reaction of Escherichia coli DNA photolyase. Proc. Natl. Acad. Sci. USA. 105:14395-14399.
34. Freire, R., U. H. Munro, L. J. Rogers, R. Wiltschko, and W. Wiltschko. 2005. Chicken orient using a magnetic compass. Curr. Biol. 15:R620-R621.
35. Wiltschko, W., R. Freire, U. Munro, T. Ritz, L. Rogers, et al. 2007. The magnetic compass of domestic chickens, Gallus gallus. J. Exp. Biol. 210:2300-2310.
36. Lohmann, K. J., N. D. Pentcheff, G. A. Nevitt, G. Stetten, R. K. Zimmer-Faust, et al. 1995. Magnetic orientation of spiny lobsters in the ocean: experiments with undersea coil systems. J. Exp. Biol. 198:2041-2048.
37. Quinn, T. P., and E. L. Brannon. 1982. The use of celestial and magnetic cues by orienting sockeye salmon fry. J. Comp. Physiol. 147:547-552.
38. Walker, M. M., C. E. Diebel, C. V. Haugh, P. M. Pankhurst, J. V. Montgomery, et al. 1997. Structure and function of the vertebrate magnetic sense. Nature. 390:371-376.
39. Diebel, C. E., R. Proksch, C. R. Green, P. Neilson, and M. M. Walker. 2000. Magnetite defines a vertebrate magnetoreceptor. Nature. 406:299-302.
40. Marhold, S., W. Wiltschko, and H. Burda. 1997. A magnetic polarity compass for direction finding in a subterranean mammal. Narurwissenschaften. 84:421-423.
41. Wang, Y., Y. Pan, S. Parsons, M. Walker, and S. Zhang. 2007. Bats respond to polarity of a magnetic field. Proc. R. Soc. Lond. B. Biol. Sci. 274:2901-2905.
42. Thalau, P., T. Ritz, H. Burda, R. E. Wegner, and R. Wiltschko. 2006. The magnetic compass mechanisms of birds and rodents are based on different physical principles. J.R. Soc. Interface. 3:583-587.
43. Wegner, R. E., S. Begall, and H. Burda. 2006. Magnetic compass in the cornea: local anaesthesia impairs orientation in a mammal. J. Exp. Biol. 209:4747-4750.
44. Fleissner, G., E. Holtkamp-Rötzler, M. Hanzlik, M. Winklhofer, G. Fleissner, et al. 2003. Ultrastructural analysis of a putative magnetore-ceptor in the beak of homing pigeons. J. Comp. Neurol. 458:350-360.
45. Fleissner, G., B. Stahl, P. Thalau, G. Falkenberg, and G. Fleissner. 2007. A novel concept of Fe- mineral based magnetoreception: Histological and physicochemical data from the upper beak of homing pigeons. Naturwissenschaften. 94:631-642.
46. Solov'yov, I. A., and W. Greiner. 2007. Theoretical analysis of an iron mineral-basedmagnetoreceptormodel in birds. Biophys. J. 93:1493-1509.
47. Beason, R. C., and P. Semm. 1996. Does the avian ophthalmic nervecarry magnetic navigational information? J. Exp. Biol. 199:1241-1244.
48. Wiltschko, R., K. Stapput, T. Ritz, P. Thalau, and W. Wiltschko. 2007. Magnetoreception in birds: different physical processes for two types of directional responses. HFSP Journal. 1:41-48.
49. Wiltschko, R., U. Munro, H. Ford, K. Stapput, and W. Wiltschko. 2008. Light-dependent magnetoreception: orientation behaviour of migratory birds under dim red light. J. Exp. Biol. 211:3344-3350.
50. Wiltschko, R., T. Ritz, K. Stapput, P. Thalau, and W. Wiltschko. 2005. Two different types of light-dependent responses to magnetic fields in birds. Curr. Biol. 15:1518-1523.
51. Mora, C. V., M. Davison, J. M. Wild, and M. M. Walker. 2004. Magnetoreception and its trigeminal mediation in the homing pigeon. Nature. 432:508-511.
52. Light, P., M. Salmon, and K. J. Lohmann. 1993. Geomagnetic orientation of loggerhead sea turtles: evidence for an inclination compass. J. Exp. Biol. 182:1-9.
53. Lohmann, K. J. 1993. Magnetic orientation by hatchling loggerhead turtles (Caretta caretta). J. Exp. Biol. 155:37-49.
54. Phillips, J. B. 1986. Two magnetoreception pathways in a migratory salamander. Science. 233:765-767.
55. Phillips, J. B., and S. C. Borland. 1992. Behavioral evidence for the use of light-dependent magnetoreception mechanism by a vertebrate. Nature. 359:142-144.
56. Phillips, J. B., and O. Sayeed. 1993. Wavelength-dependent effects of light on magnetic compass orientation in Drosophila melanogaster. J. Comp. Physiol. [A]. 172:303-308.
57. Vácha, M., and H. Soukopova. 2004. Magnetic orientation in the meal-worm beetle Tenebrio and the effect of light. J. Exp. Biol. 207:1241-1248.