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Biology Bulletin Reviews

, Volume 5, Issue 1, pp 46–62 | Cite as

Magnetoreception systems in birds: A review of current research

  • D. A. Kishkinev
  • N. S. Chernetsov
Article

Abstract

At least two independent systems of magnetoreception are currently believed to exist in birds, based on different biophysical principles, located in different parts of their bodies, and with different neuroanatomical mechanisms. One magnetoreceptory system is located in the retina, and may be based on photochemical reactions on the basis of cryptochrome. Information from these receptors is processed in a specialized part of visual Wulst, the so-called Cluster N. There are good reasons to believe that this visual magnetoreceptor processes compass magnetic information necessary for migratory orientation. The second magnetoreceptory system is probably iron-based (biogenic magnetite), located somewhere in the upper beak (its exact location and ultrastructure of receptors remain unknown) and innervated by the ophthalmic branch of trigeminal nerve. It cannot be ruled out that this system participates in spatial representation and helps forming either a kind of map or more primitive signpost sense (identification of specific geographic regions), based on regular spatial variation of the geomagnetic field. The magnetic map probably enables navigation of migrating birds across hundreds and thousands of kilometres. Apart from these two systems, whose existence has been convincingly shown (even if some details are not fully clear yet), there is evidence for the existence of magnetoreceptors based on the vestibular system. It cannot be ruled out that iron-based magnetoreception takes place in lagena (a part of inner ear in fishes, amphibians, reptiles and birds), and the information perceived is processes in vestibular nuclei. The very existence of this magnetoreception system needs verification, and its function remains completely open.

Keywords

Magnetite Trigeminal Nerve Zebra Finch Magnetic Pulse Biology Bulletin Review 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Ahmad, M. and Cashmore, A.R., HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor, Nature, 1993, vol. 366, no. 6451, pp. 162–166.PubMedGoogle Scholar
  2. Azzena, G.B., Mameli, O., and Tolu, E., Distribution of visual input to the vestibular nuclei, Arch. Ital. Biol., 1980, vol. 118, pp. 196–204.PubMedGoogle Scholar
  3. Banerjee, S.K. and Moskowitz, B.M., Ferrimagnetic properties of magnetite, in Magnetite Biomineralization and Magnetoreception in Organisms: A New Biomagnetism, Kirschvink, J.L., Jones, D.S., and McFadden, B.J., Eds., New York: Plenum, 1985, pp. 17–41.Google Scholar
  4. Batchelor, S.N., Kay, C.W.M., McLaughlan, K.A., and Shkrob, I.A., Time-resolved and modulation methods in the study of the effects of magnetic fields on the yields of free radical reactions, J. Phys. Chem., 1993, vol. 97, no. 50, pp. 13250–13258.Google Scholar
  5. Beason, R.C. and Brennan, W.J., Natural and induced magnetization in the bobolink, Dolichonyx oryzivorus (Aves: Icteridae), J. Exp. Biol., 1986, vol. 125, no. 1, pp. 49–56.Google Scholar
  6. Beason, R.C., Dussourd, N., and Deutschlander, M.E., Behavioural evidence for the use of magnetic material in magnetoreception by a migratory bird, J. Exp. Biol., 1995, vol. 198, no. 1, pp. 141–146.PubMedGoogle Scholar
  7. Beason, R.C. and Nichols, J.E., Magnetic orientation and magnetic sensitive material in a trans-equatorial migratory bird, Nature, 1984, vol. 309, no. 5964, pp. 151–153.Google Scholar
  8. Beason, R.C. and Semm, P., Magnetic responses of the trigeminal nerve system of the bobolink (Dolichonyx oryzivorus), Neurosci. Lett., 1987, vol. 80, no. 2, pp. 229–234.PubMedGoogle Scholar
  9. Beason, R.C. and Semm, P., Does the avian ophthalmic nerve carry magnetic navigational information? J. Exp. Biol., 1996, vol. 199, no. 5, pp. 1241–1244.PubMedGoogle Scholar
  10. Beason, R.C., Wiltschko, R., and Wiltschko, W., Pigeon homing: effect of magnetic pulses on initial orientation, Auk, 1997, vol. 114, no. 3, pp. 405–415.Google Scholar
  11. Beck, W. and Wiltschko, W., Magnetic factors control the migratory direction of pied flycatchers (Ficedula hypoleuca Pallas), in Proc. 19th Int. Ornithol. Congr., 1988, pp. 1955–1962.Google Scholar
  12. Berthold, P., Spatiotemporal programmes and genetics of orientation, Experientia, 1990, vol. 46, no. 4, pp. 363–371.Google Scholar
  13. Berthold, P., Spatiotemporal programmes and genetics of orientation, in Orientation in Birds, Berthold, P., Ed., Basel: Birkhauser, 1991, pp. 86–105.Google Scholar
  14. Berthold, P. and Querner, U., Genetic basis of migration behavior on European warblers, Science, 1981, vol. 212, no. 4490, pp. 77–79.PubMedGoogle Scholar
  15. Blakemore, R.P., Magnetotactic bacteria, Science, 1975, vol. 190, no. 4212, pp. 377–379.PubMedGoogle Scholar
  16. Boström, J.E., Åkesson, S., and Alerstam, T., Where on earth can animals use a geomagnetic bi-coordinate map for navigation? Ecography, 2012, vol. 35, no. 11, pp. 1039–1047.Google Scholar
  17. Cadiou, H. and McNaughton, P.A., Avian magnetite-based magnetoreception: a physiologist’s perspective, J. R. Soc. Interface, 2010, vol. 7, suppl. 2, pp. 193–205.Google Scholar
  18. Chernetsov, N., Kishkinev, D., Gashkov, S., Kosarev, V., and Bolshakov, C.V., Migratory program of juvenile pied flycatchers, Ficedula hypoleuca, from Siberia implies a detour around Central Asia, Anim. Behav., 2008b, vol. 75, no. 2, pp. 539–545.Google Scholar
  19. Chernetsov, N., Kishkinev, D., and Mouritsen, H., A long-distance avian migrant compensates for longitudinal displacement during spring migration, Curr. Biol., 2008a, vol. 18, no. 3, pp. 188–190.PubMedGoogle Scholar
  20. Diebel, C.E., Proksch, R., Green, C.R., Neilson, P., and Walker, M.M., Magnetite defines a vertebrate magnetoreceptor, Nature, 2000, vol. 406, no. 6793, pp. 299–302.PubMedGoogle Scholar
  21. Dolnik, V.R., Navigational movements of nocturnal migratory birds, Ornithologia, 1981, vol. 16, pp. 58–63.Google Scholar
  22. Emlen, S.T., Migratory orientation in the Indigo Bunting, Passerina cyanea. Part I: Evidence for use of celestial cues, Auk, 1967a, vol. 84, no. 3, pp. 309–342.Google Scholar
  23. Emlen, S.T., Migratory orientation in the Indigo Bunting, Passerina cyanea. Part II: Mechanism of celestial orientation, Auk, 1967b, vol. 84, no. 4, pp. 463–489.Google Scholar
  24. Falkenberg, G., Fleissner, G., Schuchardt, K., Kuehbacher, M., Thalau, P., Mouritsen, H., Heyers, D., Wellenreuther, G., and Fleissner, G., Avian magnetoreception: elaborate iron mineral containing dendrites in the upper beak seem to be a common feature of birds, PLoS One, 2010, vol. 5, no. 2, p. e9231.PubMedCentralPubMedGoogle Scholar
  25. Feenders, G., Liedvogel, M., Rivas, M., Zapka, M., Horita, H., Hara, E., Wada, K., Mouritsen, H., and Jarvis, E.D., Molecular mapping of movement associated areas in the avian brain: a motor theory for vocal learning origin, PLoS One, 2008, vol. 3, no. 3, p. e1768.PubMedCentralPubMedGoogle Scholar
  26. Fischer, J.H., Freake, M.J., Borland, S.C., and Phillips, J.B., Evidence for the use of magnetic map information by an amphibian, Anim. Behav., 2001, vol. 62, no. 1, pp. 1–10.Google Scholar
  27. Fischer, J.H., Munro, U., and Phillips, J.B., Magnetic navigation by an avian migrant? in Avian Migration, Berthold, P., Gwinner, E., and Sonnenschein, E., Eds., Berlin: Springer, 2003, pp. 423–432.Google Scholar
  28. Fleissner, G., Holtkamp-Rötzler, E., Hanzlik, M., Winklhofer, M., Gleissner, G., Petersen, N., and Wiltschko, W., Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons, J. Comp. Neurol., 2003, vol. 458, pp. 350–360.PubMedGoogle Scholar
  29. Fleissner, G., Stahl, B., Thalau, P., Falkenberg, G., and Fleissner, G., A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons, Naturwissenschaften, 2007, vol. 94, no. 8, pp. 631–642.PubMedGoogle Scholar
  30. Foley, L.E., Gegear, R.J., and Reppert, S.M., Human cryptochrome exhibits light-dependent magnetosensitivity, Nat. Commun., 2011, vol. 2, no. 6, p. 356.PubMedCentralPubMedGoogle Scholar
  31. Fransson, T., Jakobsson, S., Johansson, P., Kullberg, C., Lind, J., and Vallin, A., Magnetic cues trigger extensive refueling, Nature, 2001, vol. 414, no. 6859, pp. 35–36.PubMedGoogle Scholar
  32. Freake, M.J., Muheim, R., and Phillips, J.B., Magnetic maps in animals: a theory comes of age? Quart. Rev. Biol., 2006, vol. 81, no. 4, pp. 327–347.PubMedGoogle Scholar
  33. Freire, R., Dunston, E., Fowler, E.M., McKenzie, G.L., Quinn, C.T., and Michelsen, J., Conditioned response to a magnetic anomaly in the Pekin Duck (Anas platyrhynchos domestica) involves the trigeminal nerve, J. Exp. Biol., 2012, vol. 215, no. 14, pp. 2399–2404.PubMedGoogle Scholar
  34. Gagliardo, A., Ioalè, P., Savini, M., and Wild, J.M., Having the nerve to home: trigeminal magnetoreceptor versus olfactory mediation of homing in pigeons, J. Exp. Biol., 2006, vol. 209, no. 15, pp. 2888–2892.PubMedGoogle Scholar
  35. Gagliardo, A., Ioalè, P., Savini, M., and Wild, M., Navigational abilities of homing pigeons deprived of olfactory or trigeminally mediated magnetic information when young, J. Exp. Biol., 2008, vol. 211, no. 13, pp. 2046–2051.PubMedGoogle Scholar
  36. Gagliardo, A., Ioalè, P., Savini, M., and Wild, M., Navigational abilities of adult and experienced homing pigeons deprived of olfactory or trigeminally mediated magnetic information, J. Exp. Biol., 2009, vol. 212, no. 19, pp. 3119–3124.PubMedGoogle Scholar
  37. Gdowski, G.T. and McCrea, R.A., Neck proprioceptive inputs to primate vestibular nucleus neurons, Exp. Brain Res., 2000, vol. 135, no. 4, pp. 511–526.PubMedGoogle Scholar
  38. Gegear, R.J., Casselman, A., Waddell, S., and Reppert, S.M., Cryptochrome mediates light-dependent magnetosensitivity in Drosophila, Nature, 2008, vol. 454, no. 7207, pp. 1014–1018.PubMedCentralPubMedGoogle Scholar
  39. Gwinner, E. and Wiltschko, W., Endogenously controlled changes in migratory direction of the garden warbler, Sylvia borin, J. Comp. Physiol. A, 1978, vol. 125, no. 3, pp. 267–273.Google Scholar
  40. Hanzlik, M., Heunemann, C., Holtkamp-Rotzler, E., Winklhofer, M., Petersen, N., and Fleissner, G., Superparamagnetic magnetite in the upper beak tissue of homing pigeons, Biometals, 2000, vol. 13, no. 4, pp. 325–331.PubMedGoogle Scholar
  41. Harada, Y., The relation between the magnetic function of birds and fishes and their lagenal function, Acta Otolaryngol., 2008, vol. 128, no. 4, pp. 432–439.PubMedGoogle Scholar
  42. Harada, Y., Taniguchi, M., Namatame, H., and Iida, A., Magnetic materials in otoliths of bird and fish lagena and their function, Acta Otolaryngol., 2001, vol. 121, no. 5, pp. 590–595.PubMedGoogle Scholar
  43. Henshaw, I., Fransson, T., Jakobsson, S., and Kullberg, C., Geomagnetic field affects spring migratory direction in a long distance migrant, Behav. Ecol. Sociobiol., 2010, vol. 64, no. 8, pp. 1317–1323.Google Scholar
  44. Heyers, D., Manns, M., Luksch, H., Güntürkün, O., and Mouritsen, H., A visual pathway links brain structures active during magnetic compass orientation in migratory birds, PLoS One, 2007, vol. 2, no. 9, p. e937.PubMedCentralPubMedGoogle Scholar
  45. Heyers, D., Zapka, M., Hoffmeister, M., Wild, J.M., and Mouritsen, H., Magnetic field changes activate the trigeminal brainstem complex in a migratory bird, Proc. Natl. Acad. Sci. U.S.A., 2010, vol. 107, no. 20, pp. 9394–9399.PubMedCentralPubMedGoogle Scholar
  46. Hill, E. and Ritz, T., Can disordered radical pair systems provide a basis for a magnetic compass in animals? J. R. Soc. Interface, 2010, vol. 7, suppl. 2, pp. 265–271.Google Scholar
  47. Holland, R.A., Differential effects of magnetic pulses on the orientation of naturally migrating birds, J. R. Soc. Interface, 2010, vol. 7, no. 52, pp. 1617–1625.PubMedCentralPubMedGoogle Scholar
  48. Holland, R.A. and Helm, B., A strong magnetic pulse affects the precision of departure direction of naturally migrating adult but not juvenile birds, J. R. Soc. Interface, 2013, vol. 10, no. 81, p. 20121047.PubMedCentralPubMedGoogle Scholar
  49. Holland, R.A., Thorup, K., Gagliardo, A., Bisson, I.A., Knecht, E., Mizrahi, D., and Wikelski, M., Testing the role of sensory systems in the migratory heading of a songbird, J. Exp. Biol., 2009, vol. 212, no. 24, pp. 4065–4071.PubMedGoogle Scholar
  50. Ishchenko, L.A., Stolyar, S.V., Ladygina, V.P., Raikher, Yu.L., Balasoiu, M., Bayukov, O.A., Iskhakov, R.S., and Inzhevatkin, E.V., Magnetic properties and application of biomineral particles produced by bacterial culture, Phys. Proc., 2010, vol. 9, pp. 279–282.Google Scholar
  51. Kass, R.E., Ventura, V., and Cai, C., Statistical smoothing of neuronal data, Network: Comput. Neur. Syst., 2003, vol. 14, no. 1, pp. 5–15.Google Scholar
  52. Kavokin, K.V., The puzzle of magnetic resonance effect on the magnetic compass of migratory birds, Bioelectromagnetics, 2009, vol. 30, no. 5, pp. 402–410.PubMedGoogle Scholar
  53. Keary, N., Ruploh, T., Voss, J., Thalau, P., Wiltschko, R., Wiltschko, W. and Bischof, H.J., Oscillating magnetic field disrupts magnetic orientation in zebra finches, Taeniopygia guttata, Front. Zool., 2009, vol. 6, p. 25. doi:10.1186/1742-9994-6-25PubMedCentralPubMedGoogle Scholar
  54. Kirschvink, J.L., Microwave absorption by magnetite: a possible mechanism for coupling non-thermal levels of radiation to biological systems, Bioelectromagnetics, 1996, vol. 17, no. 3, pp. 187–194.PubMedGoogle Scholar
  55. Kirschvink, J.L. and Walker, M.M., Particle-size considerations for magnetite-based magnetoreceptors, in Magnetite Biomineralization and Magnetoreception in Organisms: A New Biomagnetism, Kirschvink, J.L., Jones, D.S., and McFadden, B.J., Eds., New York: Plenum, 1985, pp. 243–254.Google Scholar
  56. Kishkinev, D., Chernetsov, N., and Bolshakov, C.V., Migratory orientation of first-year pied flycatchers (Ficedula hypoleuca) from eastern Baltic, Ornithologia, 2006, vol. 33, pp. 153–160.Google Scholar
  57. Kishkinev, D., Chernetsov, N., Heyers, D., and Mouritsen, H., Migratory reed warblers need intact trigeminal nerves to correct for a 1000 km eastward displacement, PLoS One, 2013, vol. 8, no. 6, p. e65847.PubMedCentralPubMedGoogle Scholar
  58. Klarsfeld, A., Malpel, S., Michard-Vanhée, C., Picot, M., Chélot, E., and Rouyer, F., Novel features of cryptochrome-mediated photoreception in the brain circadian clock of Drosophila, J. Neurosci., 2004, vol. 24, no. 6, pp. 1468–1477.PubMedGoogle Scholar
  59. Kramer, G., Eine neue Methode zur Erforschung der Zugorientierung und die bisher damit erzielten Ergebnisse, in Proc. X Ornithol. Congr. Uppsala, 1951, pp. 269–280.Google Scholar
  60. Kramer, G., Die Sonnenorientierung der Vögel, Verh. Dtsch. Zool. Ges., Zool. Anzeig., 1953, suppl. 16, pp. 72–84.Google Scholar
  61. Kullberg, C., Henshaw, I., Jakobsson, S., Johansson, P., and Fransson, T., Fuelling decisions in migratory birds: geomagnetic cues override the seasonal effect, Proc. R. Soc. B, 2007, vol. 274, no. 1622, pp. 2145–2151.PubMedCentralPubMedGoogle Scholar
  62. Kullberg, C., Lind, J., Fransson, T., Jakobsson, S., and Vallin, A., Magnetic cues and time of season affect fuel deposition in migratory thrush nightingales (Luscinia luscinia), Proc. R. Soc. B, 2003, vol. 270, no. 1513, pp. 373–378.PubMedCentralPubMedGoogle Scholar
  63. Kuznetsov, A.N. and Vanag, V.K., Mechanism of action of magnetic fields on biological systems, Izv. Akad. Nauk SSSR, Biol., 1987, no. 6, pp. 814–827.Google Scholar
  64. Lau, J.C.S., Christopher, T.R., and Hore, P.J., Compass magnetoreception in birds arising from photo-induced radical pairs in rotationally disordered cryptochromes, J. R. Soc. Interface, 2012, vol. 9, no. 77, pp. 3329–3337.PubMedCentralPubMedGoogle Scholar
  65. Lauwers, M., Pichler, P., Edelman, N.B., Resch, G.P., Ushakova, L., Salzer, M.C., Heyers, D., Saunders, M., Shaw, J., and Keays, D.A., An iron-rich organelle in the cuticular plate of avian hair cells, Curr. Biol., 2013, vol. 23, no. 10, pp. 924–929.PubMedGoogle Scholar
  66. Liedvogel, M., Feenders, G., Wada, K., Troje, N.F., Jarvis, E.D., and Mouritsen, H., Lateralized activation of cluster N in the brains of migratory songbirds, Eur. J. Neurosci., 2007, vol. 25, pp. 1166–1173.PubMedCentralPubMedGoogle Scholar
  67. Liedvogel, M. and Mouritsen, H., Cryptochromes-a potential magnetoreceptor: what do we know and what do we want to know? J. R. Soc. Interface, 2010, vol. 7, suppl. 2, pp. 147–162.Google Scholar
  68. Liedvogel, M., Maeda, K., Henbest, K., Schleicher, E., Simon, T., Timmel, C.R., Hore, P.J., and Mouritsen, H., Chemical magnetoreception: bird cryptochrome 1a is excited by blue light and forms long-lived radical-pairs, PLoS One, 2007, vol. 2, no. 10, p. e1106.PubMedCentralPubMedGoogle Scholar
  69. Lin, C.T. and Todo, T., The cryptochromes, Genome Biol., 2005, vol. 6, p. 220. doi:10.1186/gb-2005-6-5-220PubMedCentralPubMedGoogle Scholar
  70. Liu, X. and Chernetsov, N., Avian orientation: multi-cue integration and calibration of compass systems, Chin. Birds, 2012, vol. 3, no. 1, pp. 1–8.Google Scholar
  71. Lohmann, K.J., Cain, S.D., Dodge, S.A., and Lohmann, C.M.F., Regional magnetic fields as navigational markers for sea turtles, Science, 2001, vol. 294, no. 5541, pp. 364–366.PubMedGoogle Scholar
  72. Lohmann, K.J., Hester, J.T., and Lohmann, C.M.F., Longdistance navigation in sea turtles, Ethol. Ecol. Evol., 1999, vol. 11, no. 1, pp. 1–23.Google Scholar
  73. Lohmann, K.J., Lohmann, C.M.F., Ehrhart, L.M., Bagley, D.A., and Swing, T., Geomagnetic map used in sea-turtle navigation, Nature, 2004, vol. 428, no. 6986, pp. 909–910.PubMedGoogle Scholar
  74. Lowenstam, H.A., Magnetite in denticle capping in recent chitons (Polyplacophora), Geol. Soc. Am. Bull., 1962, vol. 73, no. 4, pp. 435–438.Google Scholar
  75. Maeda, K., Henbest, K.B., Cintolesi, F., Kuprov, I., Rodgers, C.T., Liddell, P.A., Gust, D., Timmel, C.R., and Hore, P.J., Chemical compass model of avian magnetoreception, Nature, 2008, vol. 453, no. 7183, pp. 387–390.PubMedGoogle Scholar
  76. Magnetite Biomineralization and Magnetoreception in Organisms: A New Biomagnetism, Kirschvink, J.L., Jones, D.S., and McFadden, B.J., Eds., New York: Plenum, 1985.Google Scholar
  77. Möller, A., Sagasser, S., Wiltschko, W. and Schierwater, B., Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass, Naturwissenschaften, 2004, vol. 91, no. 12, pp. 585–588.PubMedGoogle Scholar
  78. Mora, C.V., Davison, M., Wild, J.M., and Walker, M.M., Magnetoreception and its trigeminal mediation in the homing pigeon, Nature, 2004, vol. 432, no. 7016, pp. 508–511.PubMedGoogle Scholar
  79. Mora, C.V. and Walker, M.M., Do release-site biases reflect response to the Earth’s magnetic field during position determination by homing pigeons? Proc. R. Soc. B, 2009, vol. 276, no. 1671, pp. 3295–3302.PubMedCentralPubMedGoogle Scholar
  80. Mora, C.V. and Walker, M.M., Consistent effect of an attached magnet on the initial orientation of homing pigeons, Columba livia, Anim. Behav., 2012, vol. 84, no. 2, pp. 377–383.Google Scholar
  81. Mouritsen, H., Search for the compass needles, Nature, 2012, vol. 484, no. 7394, pp. 320–321.PubMedGoogle Scholar
  82. Mouritsen, H. and Hore, P.J., The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds, Curr. Opin. Neurobiol., 2012, vol. 22, no. 2, pp. 343–352.PubMedGoogle Scholar
  83. Mouritsen, H., Feenders, G., Liedvogel, M., and Kropp, W., Migratory birds use head scans to detect the direction of the earth’s magnetic field, Curr. Biol., 2004a, vol. 14, no. 21, pp. 1946–1949.PubMedGoogle Scholar
  84. Mouritsen, H., Feenders, G., Liedvogel, M., Wada, K., and Jarvis, E.D., Night-vision brain area in migratory songbirds, Proc. Natl. Acad. Sci. U.S.A., 2005, vol. 102, no. 23, pp. 8339–8344.PubMedCentralPubMedGoogle Scholar
  85. Mouritsen, H., Janssen-Bienhold, U., Liedvogel, M., Feenders, G., Stalleicken, J., Dirks, P., and Weiler, R., Cryptochrome and neuroactivity markers co-localize in bird retina during magnetic orientation, Proc. Natl. Acad. Sci. U.S.A., 2004b, vol. 101, no. 39, pp. 14294–14299.PubMedCentralPubMedGoogle Scholar
  86. Muheim, R., Bäckman, J., and Åkesson, S., Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light, J. Exp. Biol., 2002, vol. 205, no. 24, pp. 3845–3856.PubMedGoogle Scholar
  87. Muheim, R., Moore, F.R., and Phillips, J.B., Calibration of magnetic and celestial compass cues in migratory birds-a review of cue-conflict experiments, J. Exp. Biol., 2006, vol. 209, no. 1, pp. 2–17.PubMedGoogle Scholar
  88. Munro, U., Munro, J.A., Phillips, J.B., and Wiltschko, W., Effect of wavelength of light and pulse magnetisation on different magnetoreception systems in a migratory bird, Aust. J. Zool., 1997a, vol. 45, no. 2, pp. 189–198.Google Scholar
  89. Munro, U., Munro, J.A., Phillips, J.B., Wiltschko, R., and Wiltschko, W., Evidence for a magnetite-based navigational ‘map’ in birds, Naturwissenschaften, 1997b, vol. 84, no. 1, pp. 26–28.Google Scholar
  90. Newton, A., A Dictionary of Birds, London: A & C Black, 1896.Google Scholar
  91. Nieβner, C., Denzau, S., Gross, J.C., Peichl, L., Bischof, H.J., Fleissner, G., Wiltschko, W. and Wiltschko, R., Avian ultraviolet/violet cones identified as probable magnetoreceptors, PLoS One, 2011, vol. 6, no. 5, p. e20091.Google Scholar
  92. Partch, C.L. and Sancar, A., Photochemistry and photobiology of cryptochrome bluelight photopigments: the search for a photocycle, Photochem. Photobiol., 2005, vol. 81, no. 6, pp. 1291–1304.PubMedGoogle Scholar
  93. Phillips, J.B., Freake, M.J., Fischer, J.H., and Borland, S.C., Behavioral titration of a magnetic map coordinate, J. Comp. Physiol. A, 2002, vol. 188, no. 2, pp. 157–160.Google Scholar
  94. Putman, N.F., Endres, C.S., Lohmann, C.M.F., and Lohmann, K.J., Longitude perception and bicoordinate magnetic maps in sea turtles, Curr. Biol., 2011, vol. 21, no. 6, pp. 463–466.PubMedGoogle Scholar
  95. Putman, N.F., Lohmann, K.J., Putman, E.M., Quinn, T.P., Klimley, A.P., and Noakes, D.L.G., Evidence for geomagnetic imprinting as a homing mechanism in Pacific salmon, Curr. Biol., 2013, vol. 23, no. 4, pp. 312–316.PubMedGoogle Scholar
  96. Rappl, R., Wiltschko, R., Weindler, P., Berthold, P., and Wiltschko, W., Orientation behavior of garden warblers, Sylvia borin, under monochromatic light of various wavelengths, Auk, 2000, vol. 117, no. 1, pp. 256–260.Google Scholar
  97. Ritz, T., Ahmad, M., Mouritsen, H., Wiltschko, R., and Wiltschko, W., Photoreceptor-based magnetoreception: optimal design of receptor molecules, cells, and neuronal processing, J. R. Soc. Interface, 2010, vol. 7, suppl. 2, pp. 135–146.Google Scholar
  98. Ritz, T., Adem, S., and Schulten, K., A model for photoreceptor-based magnetoreception in birds, Biophys. J., 2000, vol. 78, no. 2, pp. 707–718.PubMedCentralPubMedGoogle Scholar
  99. Ritz, T., Thalau, P., Phillips, J.B., Wiltschko, R., and Wiltschko, W., Resonance effects indicate a radicalpair mechanism for avian magnetic compass, Nature, 2004, vol. 429, no. 6988, pp. 177–180.PubMedGoogle Scholar
  100. Rodgers, C.T. and Hore, P.J., Chemical magnetoreception in birds: the radical pair mechanism, Proc. Natl. Acad. Sci. U.S.A., 2009, vol. 106, no. 2, pp. 353–360.PubMedCentralPubMedGoogle Scholar
  101. Sancar, A., Structure and function of DNA photolyase and cryptochromes blue-light photoreceptors, Chem. Rev., 2003, vol. 103, no. 6, pp. 2203–2237.PubMedGoogle Scholar
  102. Schmidt-Koenig, K., The sun compass, Experientia, 1990, vol. 46, no. 4, pp. 336–342.Google Scholar
  103. Schneider, T., Thalau, H.P., Semm, P., and Wiltschko, W., Melatonin is crucial for the migratory orientation of pied flycatchers (Ficedula hypoleuca Pallas), J. Exp. Biol., 1994, vol. 194, no. 1, pp. 255–262.PubMedGoogle Scholar
  104. Schulten, K., Magnetic field effects in chemistry and biology, in Festkörperprobleme, Treusch, J., Ed., Braunschweig: Vieweg, 1982, vol. 22, pp. 61–83.Google Scholar
  105. Schulten, K., Swenberg, C.E., and Weller, A., A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion, Z. Phys. Chem. (NF), 1978, vol. 111, no. 1, pp. 1–5.Google Scholar
  106. Schulten, K. and Windemuth, A., Model for a physiological magnetic compass, in Biophysical Effects of Steady Magnetic Fields, Maret, G., Boccara, N., and Kiepenheuer, J., Eds., Berlin: Springer-Verlag, 1986, vol. 11, pp. 99–106.Google Scholar
  107. Shcherbakov, V.P. and Winklhofer, M., Theoretical analysis of flux amplification by soft magnetic material in a putative biological magnetic-field receptor, Phys. Rev. E, 2010, vol. 81, no. 3, p. 031921.Google Scholar
  108. Semm, P. and Beason, R.C., Responses to small magnetic variations by the trigeminal system of the bobolink, Brain Res. Bull., 1990, vol. 25, no. 5, pp. 735–740.PubMedGoogle Scholar
  109. Solov’yov, I.A. and Greiner, W., Theoretical analysis of an iron-mineral-based magnetoreceptor model in birds, Biophys. J., 2007, vol. 93, no. 5, pp. 1493–1509.PubMedCentralPubMedGoogle Scholar
  110. Solov’yov, I., Mouritsen, H., and Schulten, K., Acuity of a cryptochrome and vision-based magnetoreception system in birds, Biophys. J., 2010, vol. 99, no. 1, pp. 40–49.PubMedCentralPubMedGoogle Scholar
  111. Stapput, K., Thalau, P., Wiltschko, R., and Wiltschko, W., Orientation of birds in total darkness, Curr. Biol., 2008, vol. 18, no. 8, pp. 602–606.PubMedGoogle Scholar
  112. Steiner, U. and Ulrich, T., Magnetic field effects in chemical kinetics and related phenomena, Chem. Rev., 1989, vol. 89, no. 1, pp. 51–147.Google Scholar
  113. Thalau, P., Ritz, T., Stapput, K., Wiltschko, R., and Wiltschko, W., Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field, Naturwissenschaften, 2005, vol. 92, no. 2, pp. 86–90.PubMedGoogle Scholar
  114. Thienemann, J., Rossitten, Neumann: Neudamm, 1927.Google Scholar
  115. Timmel, C.R. and Hore, P.J., Oscillating magnetic field effects on the yields of radical pair reactions, Chem. Phys. Lett., 1996, vol. 257, nos. 3–4, pp. 401–408.Google Scholar
  116. Treiber, C.D., Salzer, M.C., Riegler, J., Edelman, N., Sugar, C., Breuss, M., Pichler, P., Cadiou, H., Saunders, M., Lythgoe, M., Shaw, J., and Keays, D.A., Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons, Nature, 2012, vol. 484, no. 7394, pp. 367–370.PubMedGoogle Scholar
  117. Walcott, C., Anomalies in the earth’s magnetic field increase the scatter of pigeon’s vanishing bearings, in Animal Migration, Navigation, and Homing, Schmidt-Koenig, K. and Keeton, W.T., Eds., Berlin: Springer-Verlag, 1978, pp. 143–151.Google Scholar
  118. Walcott, C., Magnetic maps in pigeons, in Orientation in Birds, Berthold, P., Ed., Basel: Birkhauser, 1991, pp. 38–51.Google Scholar
  119. Walcott, C., Gould, J.L., and Kirschvink, J.L., Pigeons have magnets, Science, 1979, vol. 205, no. 4410, pp. 1027–1029.PubMedGoogle Scholar
  120. Walker, M.M., A model for encoding of magnetic-field intensity by magnetite-based magnetoreceptor cells, J. Theor. Biol., 2008, vol. 250, no. 1, pp. 85–91.PubMedGoogle Scholar
  121. Wallraff, H.G., The magnetic map of the homing pigeon, an evergreen phantom, J. Theor. Biol., 1999, vol. 197, no. 2, pp. 265–269.PubMedGoogle Scholar
  122. Wallraff, H.G., Avian Navigation: Pigeon Homing as a Paradigm, Berlin: Springer-Verlag, 2005.Google Scholar
  123. Wallraff, H.G., Kiepenheuer, J., Neumann, M.F., and Streng, A., Homing experiments with starlings deprived of the sense of smell, Condor, 1995, vol. 97, no. 1, pp. 20–26.Google Scholar
  124. Weber, S., Light-driven enzymatic catalysis of DNA repair: a review of recent biophysical studies on photolyase, BBA-Bioenergetics, 2005, vol. 1707, no. 1, pp. 1–23.PubMedGoogle Scholar
  125. Williams, M.N. and Wild, J.M., Trigeminally innervated iron-containing structures in the beak of homing pigeons, and other birds, Brain Res., 2001, vol. 889, nos. 1–2, pp. 243–246.PubMedGoogle Scholar
  126. Wiltschko, W., Further analysis of the magnetic compass of migratory birds, in Animal Migration, Navigation, and Homing, Schmidt-Koenig, K. and Keeton, W.T., Eds., Berlin: Springer-Verlag, 1978, pp. 301–310.Google Scholar
  127. Wiltschko, W., Daum, P., Fergenbauer-Kimmel, A., and Wiltschko, R., The development of the star compass in garden warblers, Sylvia borin, Ethology, 1987, vol. 74, no. 4, pp. 285–292.Google Scholar
  128. Wiltschko, W., Gesson, M., and Wiltschko, R., Magnetic compass orientation of European robins under 565 nm green light, Naturwissenschaften, 2001, vol. 88, no. 9, pp. 387–390.PubMedGoogle Scholar
  129. Wiltschko, W., Munro, U., Beason, R.C., Ford, H., and Wiltschko, R., A magnetic pulse leads to a temporary deflection in the orientation of migratory birds, Experientia, 1994, vol. 50, no. 7, pp. 697–700.Google Scholar
  130. Wiltschko, R., Munro, U., Ford, H., Stapput, K., and Wiltschko, W., Light-dependent magnetoreception: orientation behavior of migratory birds under dim red light, J. Exp. Biol., 2008, vol. 211, no. 20, pp. 3344–3350.PubMedGoogle Scholar
  131. Wiltschko, W., Munro, U., Ford, H., and Wiltschko, R., Red light disrupts magnetic orientation of migratory birds, Nature, 1993, vol. 364, no. 6437, pp. 525–527.Google Scholar
  132. Wiltschko, W., Munro, U., Ford, H., and Wiltschko, R., Effect of a magnetic pulse on the orientation of silvereyes, Zosterops l. lateralis, during spring migration, J. Exp. Biol., 1998, vol. 201, no. 23, pp. 3257–3261.PubMedGoogle Scholar
  133. Wiltschko, W., Munro, U., Ford, H., and Wiltschko, R., Avian orientation: the pulse effect is mediated by the magnetite receptors in the upper beak, Proc. R. Soc. B, 2009, vol. 276, no. 1665, pp. 2227–2232.PubMedCentralPubMedGoogle Scholar
  134. Wiltschko, R., Ritz, T., Stapput, K., Thalau, P., and Wiltschko, W., Two different types of light-dependent responses to magnetic fields in birds, Curr. Biol., 2005, vol. 15, no. 16, pp. 1518–1523.PubMedGoogle Scholar
  135. Wiltschko, R., Schiffner, I., Fuhrmann, P., and Wiltschko, W., The role of the magnetite based receptors in the beak in pigeon homing, Curr. Biol., 2010, vol. 20, no. 17, pp. 1534–1538.PubMedGoogle Scholar
  136. Wiltschko, R., Schiffner, I., and Wiltschko, W., A strong magnetic anomaly affects pigeon navigation, J. Exp. Biol., 2009, vol. 212, no. 18, pp. 2983–2990.PubMedGoogle Scholar
  137. Wiltschko, R., Stapput, K., Ritz, T., Thalau, P., and Wiltschko, W., Magnetoreception in birds: different physical processes for two types of directional responses, HFSP J., 2007, vol. 1, no. 1, pp. 41–48.PubMedCentralPubMedGoogle Scholar
  138. Wiltschko, W. and Wiltschko, R., Magnetic compass of European robins, Science, 1972, vol. 176, no. 4030, pp. 62–64.PubMedGoogle Scholar
  139. Wiltschko, W. and Wiltschko, R., Migratory orientation of European robins is affected by the wavelength of light as well as by a magnetic pulse, J. Comp. Physiol. A, 1995, vol. 177, no. 3, pp. 363–369.Google Scholar
  140. Wiltschko, W. and Wiltschko, R., The effect of yellow and blue light on magnetic compass orientation in European robins, Erithacus rubecula, J. Comp. Physiol. A, 1999, vol. 184, no. 3, pp. 295–299.Google Scholar
  141. Wiltschko, W. and Wiltschko, R., Light-dependent magnetoreception in birds: the behavior of European robins, Erithacus rubecula, under monochromatic light of various wavelengths and intensities, J. Exp. Biol., 2001, vol. 204, no. 19, pp. 3295–3302.PubMedGoogle Scholar
  142. Wiltschko, R., and Wiltschko, W., Avian navigation, Auk, 2009a, vol. 126, no. 4, pp. 717–743.Google Scholar
  143. Wiltschko, R., and Wiltschko, W., ’Fixed direction’responses of birds in the geomagnetic field, Commun. Integr. Biol., 2009b, vol. 2, no. 2, pp. 100–103.PubMedCentralPubMedGoogle Scholar
  144. Wiltschko, R., and Wiltschko, W., The magnetite-based receptors in the beak of birds and their role in avian navigation, J. Comp. Physiol. A, 2013, vol. 199, no. 2, pp. 89–98.Google Scholar
  145. Wiltschko, W., Wiltschko, R., and Munro, U., Light-dependent magnetoreception in birds: the effect of intensity of 565 nm green light, Naturwissenschaften, 2000, vol. 87, no. 8, pp. 366–369.PubMedGoogle Scholar
  146. Winklhofer, M. and Kirschvink, J.L., A quantitative assessment of torque-transducer models for magnetoreception, J. R. Soc. Interface, 2010, vol. 7, suppl. 2, pp. 273–289.Google Scholar
  147. Wu, L.-Q. and Dickman, J.D., Magnetoreception in an avian brain in part mediated by inner ear lagena, Curr. Biol., 2011, vol. 21, no. 5, pp. 418–423.PubMedCentralPubMedGoogle Scholar
  148. Wu, L.-Q. and Dickman, J.D., Neural correlates of a magnetic sense, Science, 2012, vol. 336, no. 6084, pp. 1054–1057.PubMedGoogle Scholar
  149. Zapka, M., Heyers, D., Hein, C.M., Engels, S., Schneider, N.-L., Hans, J., Weiler, S., Dreyer, D., Kishkinev, D., Wild, M., and Mouritsen, H., Visual, but not trigeminal, mediation of magnetic compass information in a migratory bird, Nature, 2009, vol. 461, no. 7268, pp. 1274–1277.PubMedGoogle Scholar
  150. Zapka, M., Heyers, D., Liedvogel, M., Jarvis, E.D., and Mouritsen, H., Night-time neuronal activation of cluster N in a day- and night-migrating songbird, Eur. J. Neurosci., 2010, vol. 32, no. 4, pp. 619–624.PubMedCentralPubMedGoogle Scholar

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© Pleiades Publishing, Ltd. 2015

Authors and Affiliations

  1. 1.Department of Integrative BiologyUniversity of GuelphGuelphCanada
  2. 2.Biological Station Rybachy, Zoological InstituteRussian Academy of SciencesRybachy, Kaliningrad oblastRussia
  3. 3.St. Petersburg State UniversitySt. PetersburgRussia

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