Magnetoreception and its use in bird navigation

Current Opinion in Neurobiology

Volumn 15, Issue 4, 2005, Pages 406-414

  Mouritsen, Henrik ^a   Ritz, Thorsten ^b  

^a UNIVERSITY OF OLDENBURG   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME; MAGNETITE;

BEAK; BEHAVIOR; BIOPHYSICS; BIRD; BRAIN; BRAIN MAPPING; CLUSTER ANALYSIS; GENE MAPPING; HEAD MOVEMENT; LIGHT EXPOSURE; MAGNETIC FIELD; MAGNETORECEPTION; MECHANORECEPTOR; MIGRATION; MOLECULE; NEUROBIOLOGY; NIGHT VISION; NONHUMAN; ORIENTATION; OSCILLATION; PHYSIOLOGY; PRIORITY JOURNAL; RETINA; REVIEW; SENSORY SYSTEM; SIGNAL DETECTION; SONGBIRD; VISION;

ANIMAL MIGRATION; ANIMALS; BEHAVIOR, ANIMAL; BIRDS; FERROSOFERRIC OXIDE; HUMANS; IRON; LIGHT; MAGNETICS; MECHANOTRANSDUCTION, CELLULAR; ORIENTATION; OXIDES;

EID: 23044443603     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2005.06.003     Document Type: Review

References (61)

1. W. Wiltschko, and R. Wiltschko Magnetic compass of European Robins Science 176 1972 62 64
2. T. Fransson, S. Jakobsson, P. Johansson, C. Kullberg, J. Lind, and A. Vallin Bird migration: magnetic cues trigger extensive refueling Nature 414 2001 35 36
3. K.J. Lohmann, S.D. Cain, S.A. Dodge, and C.M.F. Lohmann Regional magnetic fields as navigational markers for sea turtles Science 294 2001 364 366
4. M.M. Walker, T.E. Dennis, and J.L. Kirschvink The magnetic sense and its use in long-distance navigation by animals Curr Opin Neurobiol 12 2002 735 744
5. L.C. Boles, and K.J. Lohmann True navigation and magnetic maps in spiny lobsters Nature 421 2003 60 63
6. R. Wiltschko, and W. Wiltschko Magnetic Orientation In Animals 1995 Springer Verlag
7. W. Wiltschko, and R. Wiltschko Magnetic compass orientation in birds and its physiological basis Naturwissenschaften 89 2002 445 452
8. W. Wiltschko, and R. Wiltschko Pigeon homing: effect of various wavelengths of light during displacement Naturwissenschaften 85 1998 164 167
9. H. Mouritsen Redstarts, Phoenicurus phoenicurus, can orient in a true-zero magnetic field Anim Behav 55 1998 1311 1324
10. B. Cochran, H. Mouritsen, and M. Wikelski Free-flying migrating songbirds recalibrate their magnetic compass daily from sunset cues Science 304 2004 405 408 This study reports the results of the first orientation experiments with truly free-flying night-migratory birds. Night-migratory Catharus-thrushes were exposed to eastward-turned magnetic fields during the twilight period before takeoff and then followed for up to 1100 kilometres. Instead of heading north, experimental birds flew westward. On subsequent nights, the same individuals migrated northward again. Thus, the first tests with free-flying migrants suggest that they primarily use a magnetic compass in midair, but that the directional meaning of this magnetic compass is calibrated daily from sun-related cues during the twilight period. Thus, the magnetic compass is key to understanding how night-migratory birds orient during their nocturnal flights, and light measurements have set a new upper light limit, 0.0003-0.002 lux, for when a light-dependent compass must still be able to work.
11. H. Mouritsen Navigation in birds and other animals J Image Vis Comp 19 2000 713 731
12. Muheim R, Moore FR, Phillips JB: Calibration of magnetic and celestial compass cues in migratory birds - a review of cue-conflict experiments. J Exp Biol 2005, in press. A very good review of magnetic-celestial cue-conflict experiments that have been conducted with migratory birds.
13. MJ.M. Leask A physico-chemical mechanism for magnetic field detection by migratory birds and homing pigeons Nature 267 1977 144 145
14. K. Schulten, C. Swenberg, and A. Weller A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion Z Phys Chem NF111 1978 1 5
15. D. Edmonds A sensitive optically detected magnetic compass for animals Proc Biol Sci 263 1996 295 298
16. A.R. Liboff, and K.A. Jenrow New model for the avian magnetic compass Bioelectromagnetics 21 2000 555 565
17. T. Ritz, S. Adem, and K. Schulten A model for photoreceptor-based magnetoreception in birds Biophys J 78 2000 707 718
18. J.L. Kirschvink, M.M. Walker, and C.E. Diebel Magnetite-based magnetoreception Curr Opin Neurobiol 11 2001 462 467
19. R. Blakemore Magnetotactic bacteria Science 190 1975 377 379
20. M.M. Walker, C.E. Diebel, C. Haugh, P.M. Pankhurst, J.C. Montgomery, and C.R. Green Structure and function of the vertebrate magnetic sense Nature 390 1997 371 376
21. G. Fleissner, E. Holtkamp-Rotzler, M. Hanzlik, M. Winklhofer, G. Fleissner, N. Petersen, and W. Wiltschko Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons J Comp Neurol 458 2003 350 360 This paper presents the best characterization to date of a putative magnetite-based receptor structure in birds. The structure, located in the beak of pigeons, consists of super-paramagnetic particles, surrounded by ferromagnetic crystals, and is connected to the nervous system.
22. H. Mouritsen, K.P. Huyvaert, B.J. Frost, and D. Andersson Waved Albatrosses can navigate without a functional magnetic compass J Exp Biol 206 2003 4155 4166
23. F. Bonadonna, C. Bajzak, S. Benhamou, K. Igloi, P. Jouventin, H.P. Lipp, and G. Dell'Omo Orientation in the wandering albatross: interfering with magnetic perception does not affect orientation performance Proc Biol Sci 272 2005 489 495
24. Davila AF, Winklhofer M, Shcherbakov V, Petersen N: Magnetic pulse affects a putative magnetoreceptor mechanism. Biophys J 2005, in press. The authors present calculations of magnetic field effects on a superparamagnetic model magnetite receptor. Predictions from these calculations can be a valuable guide for future crucial experiments with birds, which seem to employ a structure similar to the model studied here.
25. C.V. Mora, M. Davison, J.M. Wild, and M.M. Walker Magnetoreception and its trigeminal mediation in the homing pigeon Nature 432 2004 508 511 The authors use operant conditioning to demonstrate that pigeons can detect a strong (∼100 000 nanoTesla) magnetic anomaly and that the ophthalmic branch of the trigeminal nerve carries this magnetic information to the brain. It remains to be shown that this mechanism can detect biologically relevant magnetic anomalies. Older results of Beason and Semm [26] suggest that magnetic information transmitted via the trigeminal nerve is not needed for magnetic compass orientation.
26. R. Beason, and P. Semm Does the avian ophthalmic nerve carry magnetic navigational information? J Exp Biol 199 1996 1241 1244
27. H.G. Wallraff The magnetic map of homing pigeons: an evergreen phantom J Theor Biol 197 1999 265 269
28. W. Wiltschko, U. Munro, H. Ford, and R. Wiltschko Red light disrupts magnetic orientation of migratory birds Nature 364 1993 525 527
29. W. Wiltschko, A. Möller, M. Gesson, C. Noll, and R. Wiltschko Light-dependent magnetoreception in birds: analysis of the behaviour under red light after pre-exposure to red light J Exp Biol 207 2004 1193 1202
30. R. Muheim, J. Backman, and S. Akesson Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light J Exp Biol 205 2002 3845 3856
31. W. Wiltschko, J. Traudt, O. Güntürkün, H. Prior, and R. Wiltschko Lateralization of magnetic compass orientation in a migratory bird Nature 419 2002 467 470
32. T. Schneider, H-P. Thalau, P. Semm, and W. Wiltschko Melatonin is crucial for the migratory orientation of pied flycatchers Ficedula hypoleuca pallas J Exp Biol 194 1994 255 262
33. S. Batchelor, C. Kay, K. McLaughlan, and I. Shkrob Time-resolved and modulation methods in the study of the effects of magnetic fields on the yields of free radical reactions J Phys Chem 97 1993 13250 13258
34. T. Ritz, P. Thalau, J.B. Phillips, R. Wiltschko, and W. Wiltschko Resonance effects indicate radical pair mechanism for avian magnetic compass Nature 429 2004 177 180 This study, together with that by Thalau et al. [36], reports disruptive effects of 470 nT oscillating magnetic fields in the low radio-frequency range on magnetic compass responses of migratory birds. The pattern of effects of the oscillating fields is consistent with expectations from a radical-pair mechanism [17], but cannot be reconciled easily with other mechanisms. These results represent the first, albeit indirect, evidence for a chemical magnetodetection mechanism in birds.
35. K.B. Henbest, P. Kukura, C.T. Rodgers, P.J. Hore, and C.R. Timmel Radio frequency magnetic field effects on a radical recombination reaction: a diagnostic test for the radical pair mechanism J Am Chem Soc 126 2004 8102 8103
36. P. Thalau, T. Ritz, K. Stapput, R. Wiltschko, and W. Wiltschko Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field Naturwissenschaften 92 2005 86 90
37. A. Sancar Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors Chem Rev 103 2003 2203 2237
38. A. Sancar Regulation of the mammalian clock by cryptochrome J Biol Chem 279 2004 34079 34082
39. B. Giovani, M. Byrdin, M. Ahmad, and K. Brettel Light-induced electron transfer in a cryptochrome blue-light photoreceptor Nat Struct Biol 10 2003 489 490 This study shows that plant cryptochromes can form radical pair intermediates, and it is, therefore, very likely that bird cryptochromes also form radical pairs.
40. F. Cintolesi, T. Ritz, C.W.M. Kay, C.R. Timmel, and P.J. Hore Anisotropic recombination of an immobilized photoinduced radical pair in a 50-mu T magnetic field: a model avian photomagnetoreceptor Chem Phys 294 2003 385 399
41. Z. Fu, M. Inaba, T. Noguchi, and H. Kato Molecular cloning and circadian regulation of cryptochrome genes in Japanese quail (Coturnix coturnix japonica) J Biol Rhythms 17 2002 14 27
42. R. Haque, S.S. Chaurasia, J.H. Wessel III, and P.M. Iuvone Dual regulation of cryptochrome I mRNA expression in chicken retina by light and circadian oscillators Neuroreport 13 2002 2247 2251
43. H. Mouritsen, U. Janssen-Bienhold, M. Liedvogel, G. Feenders, J. Stalleicken, P. Dirks, and R. Weiler Cryptochromes and activity markers co-localize in bird retina during magnetic orientation Proc Natl Acad Sci USA 101 2004 14294 14299 The authors show that cryptochromes are found in the retinae of night-migratory birds and map the cellular location of cryptochrome within the retinae. The authors also show that the retinal ganglion cells and displaced ganglion cells, which also contain lots of cryptochrome, show high levels of neuronal activity during magnetic orientation in migratory birds. Furthermore, the authors found clear differences in cryptochrome expression and neuronal activity between migratory garden warblers and non-migratory zebra finches, which support the suggestion that cryptochromes could be the primary sensor for the magnetic compass in migratory birds.
44. A. Möller, S. Sagasser, W. Wiltschko, and B. Schierwater Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass Naturwissenschaften 91 2004 585 588 The authors demonstrate that cryptochromes are found in the retinae of a night-migratory bird, the European robin.
45. K. Fite, M. Brecha, H. Karten, and S. Hunt Displaced ganglion cells and the accessory optics system of pigeons J Comp Neurol 195 1981 279 288
46. L.R.G. Britto, K.T. Keyser, D.E. Hamassaki, and H.J. Karten Catecholaminergic subpopulation of retinal displaced ganglion cells projects to the accessory optic nucleus in the pigeon (Columba livia) J Comp Neurol 269 1988 109 117
47. P. Semm, and C. Demaine Neurophysiological properties of magnetic cells in the pigeon's visual system J Comp Physiol [A] 159 1986 619 625
48. P. Nemec, J. Altmann, S. Marhold, H. Burda, and H. Oelschläger Neuroanatomy of magnetoreception: the superior colloculus involved in magnetic orientation in a mammal Science 294 2001 366 368
49. P. Nemec, H. Burda, and H. Oelschläger Towards the neural basis of magnetoreception: a neuroanatomical approach Naturwissenschaften 92 2005 151 157
50. H. Mouritsen, G. Feenders, M. Liedvogel, K. Wada, and E.D. Jarvis A night vision brain area in migratory songbirds Proc Natl Acad Sci USA 102 2005 8339 8344 The authors used sensory-driven gene expression to show that night migratory songbirds possess a tight cluster of brain regions, 'cluster N', that are highly active only during night-vision, because the activity in cluster N disappeared in migrants when both eyes were covered. By contrast, neuronal activation of cluster N was not increased in non-migratory birds, neither during the day nor during the night. The discovery of a seemingly specialized distinct night-vision brain area in night-migratory songbirds supports the idea that they process magnetically modulated visual signals at night.
51. E.D. Jarvis, and F. Nottebohm Motor-driven gene expression Proc Natl Acad Sci USA 94 1997 4097 4102
52. E.D. Jarvis Brains and birdsong P. Marler H. Slabbekoorn Nature's Music: The Science of Birdsong 2004 Elsevier-Academic Press 239 275
53. C.V. Mello, and D.F. Clayton Differential induction of the ZENK gene in the avian forebrain and song control circuit after metrazole-induced depolarization J Neurobiol 26 1995 145 161
54. H. Mouritsen, G. Feenders, M. Liedvogel, and W. Kropp Migratory birds use head scans to detect the direction of the Earth's magnetic field Curr Biol 14 2004 1946 1949 The authors observed that caged migratory garden warblers performed head scanning behaviour, which seemed to be used by the birds to detect the reference compass direction of the geomagnetic field. The implications are that the primary magnetic compass detector must be located in the head region, and that the magnetic compass sense of birds relies on relative measures to detect the magnetic reference compass direction.
55. Wylie DRW, W.F. Bischof, and B.J. Frost Common reference frame for neural coding of translational and rotational optic flow Nature 392 1998 278 282
56. W. Wiltschko, U. Munro, H. Ford, and R. Wiltschko Magnetic orientation in birds: non-compass responses under monochromatic light of increased intensity Proc Biol Sci 270 2003 2133 2140 In this study and two others by this group [ 29,57 ], the authors show that magnetic compass responses under light with various wavelengths are much more complicated than first anticipated. The findings strongly suggest that more than one type of receptor molecule is involved in magnetic compass detection.
57. W. Wiltschko, M. Gesson, K. Stapput, and R. Wiltschko Light-dependent magnetoreception in birds: interaction of at least two different receptors Naturwissenschaften 91 2004 130 134
58. T. Ritz, D.H. Dommer, and J.B. Phillips Shedding light on vertebrate magnetoreception Neuron 34 2002 503 506
59. P. Berthold A comprehensive theory for the evolution, control and adaptability of avian migration Ostrich 70 1999 1 11
60. H. Mouritsen Spatiotemporal orientation strategies of long-distance migrants P. Berthold E. Gwinner E. Sonnenschein Avian Migration 2003 Springer Verlag 493 513
61. H. Mouritsen, and O. Mouritsen A mathematical expectation model for bird navigation based on the clock-and-compass strategy J Theor Biol 207 2000 283 291