Magnetic orientation and magnetoreception in birds and other animals

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 191, Issue 8, 2005, Pages 675-693

  Wiltschko, Wolfgang ^a   Wiltschko, Roswitha ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BIRD; MAGNETISM; ORIENTATION; PHYSIOLOGY; POPULATION MIGRATION; REVIEW;

ANIMAL MIGRATION; ANIMALS; BIRDS; MAGNETICS; ORIENTATION;

EID: 23944456116     PISSN: 03407594     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00359-005-0627-7     Document Type: Review

References (106)

1. Baker RR (1989) Human navigation and magnetoreception. Manchester University Press, Manchester and New York
2. Beason RC, Brennon WJ (1986) Natural and induced magnetization in the bobolink (Dolichonyx orycivorus). Ethology 91:75-80
3. Beason RC, Nichols JE (1984) Magnetic orientation and magnetically sensitive material in a transequatorial migratory bird. Nature 309:151-153
4. Beason RC, Semm P (1991) Two different magnetic systems in avian orientation. In: Bell BD, Cossee RO, Flux JEC, Heather BD, Hitchmough RA, Robertson CJR, Williams MJ (eds) Acta XX Congr Intern Ornithol, New Zealand Ornithological Congress Trust Board, Wellington, pp 1813-1819
5. Beason RC, Semm P (1996) Does the avian ophthalmic nerve carry magnetic navigational information? J Exp Biol 199:1241-1244
6. Beason RC, Dussourd N, Deutschlander M (1995) Behavioural evidence for the use of magnetic material in magnetoreception by a migratory bird. J Exp Biol 198:141-146
7. Beason RC, Wiltschko R, Wiltschko W (1997) Pigeon homing: effects of magnetic pulses on initial orientation. Auk 114:405-415
8. Beck W, Wiltschko W (1988) Magnetic factors control the migratory direction of Pied Flycatchers (Ficedula hypoleuca Pallas). In: Ouellet H (ed) Acta XIX Congr Int Ornithol Vol II. University of Ottawa Press, Ottawa, pp 1955-1962
9. Blakemore RP (1975) Magnetotactic bacteria. Science 190:377-379
10. Boles LC, Lohmann KJ (2003) True navigation and magnetic map in spiny lobsters. Nature 421:60-63
11. Cranfield J, Belford R, Debrunner P, Schulten K (1994) A perturbation treatment of oscillating magnetic fields in the radical pair mechanism. Chem Phys 182:1-18
12. Davila AF, Winklhofer M, Sheherbakov V, Petersen N Magnetic pulse affects a putative magnetoreceptor mechanism. Biophys J in press
13. DeJong D (1982) Orientation of comb building by honeybees. J Comp Physiol 147:495-501
14. Deutschlander ME, Phillips JB, Borland SC (1999) The case for light-dependent magnetic orientation in animals. J Exp Biol 202:891-908
15. Diebel CE, Proksch R, Green CR, Neilson P, Walker MM (2000) Magnetite defines a vertebrate magnetoreceptor. Nature 406:299-302
16. Duelli P, Duelli-Klein R (1978) Die magnetische Nestausrichtung der australischen Kompaßtermite Amitermes meridionalis. Mitt Schweiz Entomol Ges 51:337-342
17. Edmonds DT (1996) A sensitive optically detected magnetic compass for animals. Proc R Soc Lond B 263:295-298
18. Fisher JH, Munro U, Phillips JB (2003) Magnetic navigation in an avian migrant? In: Berthold P, Gwinner E, Sonnenschein E (ed) Avian migration. Springer, Berlin Heidelberg New York, pp 423-432
19. Fleissner G, Holtkamp-Rötzler E, Hanzlik M, Winklhofer M, Fleissner G, Petersen N, Wiltschko W (2003) Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J Comp Neurol 458:350-360
20. Fransson T, Jakobsson S, Johansson P, Kullberg C, Lind J, Vallin A (2001) Magnetic cues trigger extensive refuelling. Nature 414:35-36
21. Giovani B, Byrdin M, Ahmad M, Brettel K (2003) Light-induced electron transfer in a cryptochrome blue-light photoreceptor. Nature Struct Biol 6:489-490
22. Gould JL, Kirschvink JL, Deffeyes KS (1978) Bees have magnetic remanence. Science 201:1026-1028
23. Gundmundsson GA, Sandberg R (2000) Sanderlings (Calidris alba) have a magnetic compass: orienation experiments during spring migration in Iceland. J Exp Biol 203:3137-3144
24. Güntürkün O (1997) Morphological asymmetries of the tectum opticum in the pigeon. Exp Brain Res 116:561-566
25. Hanzlik M, Heunemann C, Holzkamp-Rötzler E, Winklhofer M, Petersen N, Fleissner G (2000) Superparamagnetic magnetite in the upper beak tissue of homing pigeons. BioMetals 13:325-331
26. Haque R, Charausia SS, Wessel JH, Iuvone PM (2002) Dual regulation of cryptochrome I mRNA expression in chicken retina by light and circadian oscillators. Neuroreport 13:2247-2251
27. Henbest KB, Kukura P, Rodgers CT, Hore PJ, Timmel CR (2004) Radio frequency magnetic field effects on a radical recombination reaction: a diagnostic test for the radical pair mechanism. J Am Chem Soc 126:8102-8103
28. Jacklyn PM, Munro U (2002) Evidence for the use of magnetic cues in mound construction by the termite Amitermes meridionalis (Isoptera, Termitinae). Austr J Zool 50:357-368
29. Kalmijn AJ (1978) Electric and magnetic sensory world of sharks, skates, and rays. In: Hodgson FS, Mathewson RF (eds) Sensory biology of sharks, skates and rays. Office Naval Res, Arlington, VA, pp 507-528
30. Keeton WT, Larkin TS, Windsor DM (1974) Normal fluctuation in the earth's magnetic field influence pigeon orientation. J Comp Physiol 95:95-103
31. Kirschvink JL, Gould JL (1981) Biogenetic magnetite as a basis for magnetic field detection in animals. BioSystems 13:181-201
32. Kirschvink JL, Walker MM (1985) Particle-size considerations for magnetite-based magnetoreceptors. In: Kirschvink JL, Jones DS, MacFadden BJ (eds) Magnetite biomineralization and magnetoreception in organisms. Plenum, New York, London, pp 243-256
33. Kirschvink JL, Jones DS, MacFadden BJ (eds) (1985) Magnetite biomineralization and magnetoreception in organisms. Plenum, New York
34. Light P, Salmon M, Lohmann KJ (1993) Geomagnetic orientation of loggerhead sea turtles: evidence for an inclination compass. J Exp Biol 182:1-10
35. Lohmann KJ (1991) Magnetic orientation by hatchling loggerhead sea turtles (Caretta caretta). J Exp Biol 155:37-49
36. Lohmann KJ, Lohmann CMF (1992) Orientation to oceanic waves by green turtle hatchlings. J Exp Biol 171:1-13
37. Lohmann KJ, Lohmann CMF (1993) A light-independent magnetic compass in the leatherback sea turtle. Biol Bull 185:149-151
38. Lohmann KJ, Lohmann CMF (1994) Detection of magnetic inclination angle by sea turtles: a possible mechanism for determining latitudes. J Exp Biol 194:23-32
39. Lohmann KJ, Lohmann CMF (1996) Detection of magnetic field intensity by sea turtles. Nature 380:59-61
40. Lohmann KJ, Pentcheff ND, Nevitt GA, Stetten GD, Zimmer-Faust RK, Jarrard HE, Boles LC (1995) Magnetic orientation of spiny lobsters in the ocean: experiments with underseas coil systems. J Exp Biol 198:2041-2048
41. Lohmann KJ, Cain SD, Dodge SA, Lohmann CMF (2001) Regional magnetic fields as navigational markers for sea turtles. Science 294:364-366
42. Lohmann KJ, Lohmann CMF, Erhart LM, Bagley DA, Swing T (2004) Geomagnetic map used in sea-turtle navigation. Nature 428:909-910
43. Mai JK, Semm P (1990) Patterns of glucose utilization following magnetic stimulation. J Hirnforsch 31:331-336
44. Maier EJ (1992) Spectral sensitivities including the ultraviolet of the passeriform bird Leiothrix lutea. J Comp Physiol A 170:709-714
45. Mann S, Sparks NHC, Walker MM, Kirschvink JL (1988) Ultrastructure, morphology and organization of biogenic magnetite from Sockeyes salmon, Oncorhynchus nerka: implications for magnetoreception. J Exp Biol 140:35-49
46. Marhold S, Burda H, Wiltschko W (1997a) A magnetic polarity compass for direction finding in a subterranean mammal. Naturwissenschaften 84:421-423
47. Marhold S, Burda H, Kreilos I, Wiltschko W (1997b) Magnetic orientation in the common mole-rat from Zambia. In: Orientation and navigation - birds, humans and other animals. Royal Instit of Navig, Oxford, 5-1-5-9
48. 2-based blue-light photoreceptors in the retinohypothalamic tract as the photoactive pigments for setting the circadian clock in mammals. Proc Natl Acad Sci USA 95:6097-6102
49. Möller A, Gesson M, Noll C, Phillips J, Wiltschko R, Wiltschko W (2001) Light-dependent magnetoreception in migratory birds previous exposure to red light alters the response to red light. In: Orientation and navigation - birds, humans and other animals. Royal Institute of Navigation, Oxford, 6-1-6-6
50. Möller A, Sagasser S, Wiltschko W, Schierwater B (2004) Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass. Naturwissenschaften 91:585-588
51. Mora CV, Davison M, Wild JM, Walker MM (2004) Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432:508-511
52. Mouritsen H, Janssen-Bienhold U, Liedvogel M, Feenders G, Stalleicken J, Dirks P, Weiler R (2004) Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proc Nat Acad Sci USA 101:14294-14299
53. Muheim R, Bäckman J, Åkesson S (2002) Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light. J Exp Biol 205:3845-3856
54. Munro U, Munro JA, Phillips JB, Wiltschko R, Wiltschko W (1997) Evidence for a magnetite-based navigational 'map' in birds. Naturwissenschaften 84:26-28
55. Murray RW (1962) The response of the ampullae of Lorenzini of elasmobranchs to electrical stimulation. J Exp Biol 39:119-128
56. Němec P, Altmann J, Marhold S, Burds H, Oelschläger HHA (2001) Neuroanatomy of magnetoreception: the superior colliculus involved in magnetic orientation in a mammal. Science 294:366-368
57. Pardi L, Ugolini A, Faqi AS, Scapini F, Ercolini A (1988) Zonal recovering in equatorial sandhoppers: Interaction between magnetic and solar orientation. In: Chelazzi G, Vannini M (eds) Behavioral adaptation to intertidal life. Proc of the NATO Sci, Plenum, New York, London, pp 79-92
58. Phillips JB (1986) Two magnetoreception pathways in a migratory salamander. Science 233:765-767
59. Phillips JB, Borland SC (1992a) Magnetic compass orientation is eliminated under near-infrared light in the eastern red-spotted newt Notophthalmus viridescens. Anim Behav 44:796-797
60. Phillips JB, Borland SC (1992b) Behavioral evidence for use of a light-dependent magnetoreception mechanism by a vertebrate. Nature 359:142-144
61. Phillips JB, Borland SC (1994) Use of a specialized magnetoreception system for homing by the eastern red-spotted newt Notophthalmus viridescens. J Exp Biol 188:275-291
62. Phillips JB, Deutschlander ME (1997) Magnetoreception in terrestrial vertebrates: implications for possible mechanisms of EMF interaction with biological systems. In: Stevens RG, Wilson BW, Andrews LE (eds) The melatonin hypothesis: electric power and the risk of breast cancer. Battelle Press, Columbus Ohio, pp 111-172
63. Phillips JB, Deutschlander ME, Freake MJ, Borland SC (2001) The role of extraocular photoreceptors in newt magnetic compass orientation: parallels between light-dependent magnetoreception and polarized light detection in vertebrates. J Exp Biol 204:2543-2552
64. Phillips JB, Freake MJ, Borland SC (2002a) Behavioral titration of magnetic map coordinates. J Comp Physiol A 188:157-160
65. Phillips JB, Borland SC, Freake M, Brassart J, Kirschvink JL (2002b) 'Fixed-axis' magnetic orientation by an amphibian: non-shoreward-directed compass orientation, misdirected homing or positioning a magnetite-based map detector in a consistent alignment relative to the magnetic field? J Exp Biol 205:3903-3914
66. Prior H, Wiltschko R, Stapput K, Güntürkün O, Wiltschko W (2004) Visual lateralization and homing in pigeons. Behav Brain Res 154:301-310
67. Quinn TP (1980) Evidence for celestial and magnetic compass orientation in lake migrating sockeye salmon fry. J Comp Physiol 137:243-248
68. Quinn TP, Brannon EL (1982) The use of celestial and magnetic cues by orienting sockeye salmon smolts. J Comp Physiol 147:547-552
69. Ritz T, Adem S, Schulten K (2000) A model for vision-based magnetoreception in birds. Biophys J 78:707-718
70. Ritz T, Thalau P, Phillips JB, Wiltschko R, Wiltschko W (2004) Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429:177-180
71. Sancar A (2003) Structure and function of DNA photolyase and cryptochrome blue-light photorceptors. Chem Rev 103:2203-2237
72. Schulten K, Windemuth A (1986) Model for a physiological magnetic compass. In: Maret G, Boccara N, Kiepenheuer J (eds). Biophysical effects of steady magnetic fields. Springer, Berlin Heidelberg New York, pp 99-106
73. Semm P, Beason RC (1990) Responses to small magnetic variations by the trigeminal system of the Bobolink. Brain Res Bull 25:735-740
74. Semm P, Demaine C (1986) Neurophysiological properties of magnetic cells in the pigeon's visual system. J Comp Physiol A 159:619-625
75. Semm P, Nohr D, Demaine C, Wiltschko W (1984) Neural basis of the magnetic compass: interaction of visual, magnetic and vestibular inputs in the pigeons's brain. J Comp Physiol 155:283-288
76. Shcherbakov VP, Winklhofer M (1999) The osmotic magnetometer: a new model for magnetite-based magnetoreceptors in animals. Eur Biophys J 28:380-392
77. Skiles DD (1985) The geomagnetic field: its nature, history and biological relevance. In: Kirschvink JL, Jones DS MacFadden BJ (eds) Magnetite biomineralization and magnetoreception in organisms. Plenum, New York, London, pp 43-102
78. Stapput K, Gesson M, Wiltschko R, Wiltschko W (2005) Light-dependent magnetoreception: behavior of migratory birds under monochromatic and bichromatic lights. In: Orientation and Navigation. Proc RIN 05 Conf, Royal Institute of Navigation, Reading (in press)
79. Thalau P, Ritz T, Stapput K, Wiltschko R, Wiltschko W (2005) Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften 92:86-90
80. Viguier C (1882) Le sens de l'orientation et ses organes chez les animaux et chez l'homme. Revue Philosophique de la France et de l'Étranger 14:1-36
81. Walcott C (1978) Anomalies in the earth's magnetic field increase the scatter of pigeons' vanishing bearings. In: Schmidt-Koenig K, Keeton WT (eds) Animal migration, navigation and homing. Springer, Berlin Heidelberg New York, pp 143-151
82. Walcott C, Green RP (1974) Orientation of homing pigeons alterd by a change in the direction of an applied magnet field. Science 184:180-182
83. Walker MM, Diebel CE, Haugh CV, Pankhurst PM, Montgomery JC Green CR (1997) Structure and function of the vertebrate magnetic sense. Nature 390:371-376
84. Williams MN, Wild JM (2001) Trigeminally innervated iron-containing structures in the beak of homing pigeons and other birds. Brain Res 889:243-246
85. Wiltschko W (1978) Further analysis of the magnetic compass of migratory birds. In: Schmidt-König K, Keeton WT (eds) Animal migration, navigation and homing. Springer, Berlin Heidelberg New York, pp 302-310
86. Wiltschko W, Wiltschko R (1972) Magnetic compass of European Robins. Science 176:62-64
87. Wiltschko R, Wiltschko W (1978) Evidence for the use of magnetic outward-journey information in homing pigeons. Naturwissenschaften 65:112
88. Wiltschko W, Wiltschko R (1981) Disorientation of inexperienced young pigeons after transportation in total darkness. Nature 291:433-434
89. Wiltschko W, Wiltschko R (1992) Migratory orientation: magnetic compass orientation of Garden Warblers (Sylvia borin) after a simulated crossing of the magnetic equator. Ethology 91:70-79
90. Wiltschko R, Wiltschko W (1995) Magnetic Orientation in Animals. Springer, Berlin Heidelberg New York
91. Wiltschko W, Wiltschko R (1999) The effect of yellow and blue light on magnetic compass orientation in European Robins, Erithacus rubecula. J Comp Physiol A 184:295-299
92. Wiltschko W, Wiltschko R (2001) Light-dependent magnetoreception in birds: the behavior of European Robins, Erithacus rubecula, under monochromatic light of various wavelengths. J Exp Biol 204:3295-3302
93. Wiltschko W, Wiltschko R (2002) Magnetic compass orientation in birds and its physiological basis. Naturwissenschaften 89:445-452
94. Wiltschko R, Wiltschko W (2003) Avian navigation: from historical to modern concepts. Anim Behav 65:257-272
95. Wiltschko W, Munro U, Ford H, Wiltschko R (1993) Red light disrupts magnetic orientation of migratory birds. Nature 364:525-527
96. Wiltschko W, Munro U, Beason RC, Ford H, Wiltschko R (1994) A magnetic pulse leads to a temporary deflection in the orientation of migratory birds. Experientia 50:697-700
97. Wiltschko W, Munro U, Ford H, Wiltschko R (1998) Effect of a magnetic pulse on the orientation of Silvereyes, Zosterops l. lateralis, during spring migration. J Exp Biol 201:3257-3261
98. Wiltschko W, Wiltschko R, Munro U (2000) Light-dependent magnetoreception in birds: the effect of intensity of 565-nm green light. Naturwissenschaften 87:366-369
99. Wiltschko W, Gesson M, Wiltschko R (2001) Magnetic compass orientatiom of European robins under 565 nm green light. Naturwissenschaften 88:387-390
100. Wiltschko W, Traudt J, Güntürkün O, Prior H, Wiltschko R (2002a) Lateralization of magnetic compass orientation in a migratory bird. Nature 419:467-470
101. Wiltschko W, Munro U, Wiltschko W, Kirschvink JL (2002b) Magnetite-based magnetoreception in birds: the effect of a biasing field and a pulse on migratory behavior. J Exp Biol 205:3031-3037
102. Wiltschko W, Munro U, Ford H, Wiltschko R (2003a) Lateralisation of magnetic compass orientation in silvereyes, Zosterops lateralis. Austr J Zool 51:1-6
103. Wiltschko W, Munro U, Ford H, Wiltschko R (2003b) Magnetic orientation in birds: non-compass responses under monochromatic light of increased intensity. Proc R Soc Lond B 270:2133-2140
104. Wiltschko W, Möller A, Gesson M, Noll C, Wiltschko R (2004a) Light-dependent magnetoreception in birds analysis of the behaviour under red light after pre-exposure to red light. J Exp Biol 207:1193-1202
105. Wiltschko W, Gesson M, Stapput K, Wiltschko R (2004b) Light-dependent magnetoreception in birds: interaction of at least two different receptors. Naturwissenschaften 91:130-134
106. Yorke ED (1979) A possible magnetic transducer in birds. J Theor Biol 77:101-105