Skip to main content
SpringerLink
Log in

Magnetoreception systems in birds: A review of current research

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • Berthold, P., Spatiotemporal programmes and genetics of orientation, Experientia, 1990, vol. 46, no. 4, pp. 363–371.

    Google Scholar 

  • Berthold, P., Spatiotemporal programmes and genetics of orientation, in Orientation in Birds, Berthold, P., Ed., Basel: Birkhauser, 1991, pp. 86–105.

    Google Scholar 

  • Berthold, P. and Querner, U., Genetic basis of migration behavior on European warblers, Science, 1981, vol. 212, no. 4490, pp. 77–79.

    CAS  PubMed  Google Scholar 

  • Blakemore, R.P., Magnetotactic bacteria, Science, 1975, vol. 190, no. 4212, pp. 377–379.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Dolnik, V.R., Navigational movements of nocturnal migratory birds, Ornithologia, 1981, vol. 16, pp. 58–63.

    Google Scholar 

  • 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 

  • 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 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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:10.1186/1742-9994-6-25

    PubMed Central  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • Kramer, G., Die Sonnenorientierung der Vögel, Verh. Dtsch. Zool. Ges., Zool. Anzeig., 1953, suppl. 16, pp. 72–84.

    Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • Lin, C.T. and Todo, T., The cryptochromes, Genome Biol., 2005, vol. 6, p. 220. doi:10.1186/gb-2005-6-5-220

    PubMed Central  PubMed  Google Scholar 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • Lowenstam, H.A., Magnetite in denticle capping in recent chitons (Polyplacophora), Geol. Soc. Am. Bull., 1962, vol. 73, no. 4, pp. 435–438.

    CAS  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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 

  • Mouritsen, H., Search for the compass needles, Nature, 2012, vol. 484, no. 7394, pp. 320–321.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • Newton, A., A Dictionary of Birds, London: A & C Black, 1896.

    Google Scholar 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sancar, A., Structure and function of DNA photolyase and cryptochromes blue-light photoreceptors, Chem. Rev., 2003, vol. 103, no. 6, pp. 2203–2237.

    CAS  PubMed  Google Scholar 

  • Schmidt-Koenig, K., The sun compass, Experientia, 1990, vol. 46, no. 4, pp. 336–342.

    Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Schulten, K., Magnetic field effects in chemistry and biology, in Festkörperprobleme, Treusch, J., Ed., Braunschweig: Vieweg, 1982, vol. 22, pp. 61–83.

    Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Steiner, U. and Ulrich, T., Magnetic field effects in chemical kinetics and related phenomena, Chem. Rev., 1989, vol. 89, no. 1, pp. 51–147.

    CAS  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Thienemann, J., Rossitten, Neumann: Neudamm, 1927.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • Walcott, C., Magnetic maps in pigeons, in Orientation in Birds, Berthold, P., Ed., Basel: Birkhauser, 1991, pp. 38–51.

    Google Scholar 

  • Walcott, C., Gould, J.L., and Kirschvink, J.L., Pigeons have magnets, Science, 1979, vol. 205, no. 4410, pp. 1027–1029.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Wallraff, H.G., The magnetic map of the homing pigeon, an evergreen phantom, J. Theor. Biol., 1999, vol. 197, no. 2, pp. 265–269.

    PubMed  Google Scholar 

  • Wallraff, H.G., Avian Navigation: Pigeon Homing as a Paradigm, Berlin: Springer-Verlag, 2005.

    Google Scholar 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • Wiltschko, W. and Wiltschko, R., Magnetic compass of European robins, Science, 1972, vol. 176, no. 4030, pp. 62–64.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • Wiltschko, R., and Wiltschko, W., Avian navigation, Auk, 2009a, vol. 126, no. 4, pp. 717–743.

    Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wu, L.-Q. and Dickman, J.D., Neural correlates of a magnetic sense, Science, 2012, vol. 336, no. 6084, pp. 1054–1057.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Integrative Biology, University of Guelph, Guelph, Canada, N1G 2W1

    D. A. Kishkinev

  2. Biological Station Rybachy, Zoological Institute, Russian Academy of Sciences, Rybachy, Kaliningrad oblast, 238535, Russia

    N. S. Chernetsov

  3. St. Petersburg State University, Universitetskaya nab. 7/9, St. Petersburg, 199034, Russia

    N. S. Chernetsov

Authors
  1. D. A. Kishkinev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. S. Chernetsov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. S. Chernetsov.

Additional information

Published in Russian in Zhurnal Obshchei Biologii, 2014, Vol. 75, No. 2, pp. 104–123.

The article was translated by the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kishkinev, D.A., Chernetsov, N.S. Magnetoreception systems in birds: A review of current research. Biol Bull Rev 5, 46–62 (2015). https://doi.org/10.1134/S2079086415010041

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086415010041

Keywords

Search

Navigation