Magnetoreception in birds: two receptors for two different tasks

Birds can use the geomagnetic field as a source of navigational information in different ways: the magnetic vector provides a compass; magnetic intensity and/or inclination play a role as a component of the navigational ‘map’, and magnetic conditions of certain regions act as ‘sign posts’ or triggers, eliciting specific responses. Two hypotheses on magnetoreception are currently under discussion. One proposes a chemical compass based on a radical pair mechanism involving direction-dependent reactions in specialized photopigments; the other postulates processes involving iron-rich particles, such as magnetite. Behavioral evidence suggests that birds use both mechanisms, with radical pair processes in the right eye providing directional information and an iron-based mechanism in the upper beak providing information on position as a component of the navigational ‘map’. Electrophysiological data support this view. The interactions of the two mechanisms, however, are still poorly understood.

[1]  R. Beason,et al.  Natural and Induced Magnetization in the Bobolink, Dolichonyx Oryzivorus (Aves: Icteridae) , 1986 .

[2]  Wolfgang Wiltschko,et al.  Light-dependent magnetoreception in birds: interaction of at least two different receptors , 2004, Naturwissenschaften.

[3]  M. Winklhofer,et al.  The osmotic magnetometer: a new model for magnetite-based magnetoreceptors in animals , 1999, European Biophysics Journal.

[4]  Wolfgang Wiltschko,et al.  Magnetic compass orientation in birds and its physiological basis , 2002, Naturwissenschaften.

[5]  L. Rogers,et al.  Chickens orient using a magnetic compass , 2005, Current Biology.

[6]  Michael J. Bailey,et al.  Chickens’ Cry2: molecular analysis of an avian cryptochrome in retinal and pineal photoreceptors , 2002, FEBS letters.

[7]  J. Lind,et al.  Magnetic cues and time of season affect fuel deposition in migratory thrush nightingales (Luscinia luscinia) , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[8]  W. Wiltschko,et al.  Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons , 2003, The Journal of comparative neurology.

[9]  W. Wiltschko,et al.  Magnetic orientation in birds: non–compass responses under monochromatic light of increased intensity , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  Joseph L. Kirschvink,et al.  Particle-Size Considerations for Magnetite-Based Magnetoreceptors , 1985 .

[11]  Wolfgang Wiltschko,et al.  Magnetite-based magnetoreception in birds: the effect of a biasing field and a pulse on migratory behavior. , 2002, The Journal of experimental biology.

[12]  W. Wiltschko,et al.  Magnetic Compass of European Robins , 1972, Science.

[13]  Wolfgang Wiltschko,et al.  Avian navigation: from historical to modern concepts , 2003, Animal Behaviour.

[14]  H. Bischof,et al.  The use of the geomagnetic field for short distance orientation in zebra finches , 2007, Neuroreport.

[15]  Geographic song variation within and between populations and subspecies of the rufous bristlebird, Dasyornis broadbenti , 2003 .

[16]  W. Wiltschko,et al.  Neural basis of the magnetic compass: interactions of visual, magnetic and vestibular inputs in the pigeon's brain , 1984, Journal of Comparative Physiology A.

[17]  M. Bookman,et al.  Sensitivity of the homing pigeon to an Earth-strength magnetic field , 1977, Nature.

[18]  Dr. Roswitha Wiltschko,et al.  Magnetic Orientation in Animals , 1995, Zoophysiology.

[19]  L. Rogers,et al.  Lateralized response of chicks to magnetic cues , 2008, Behavioural Brain Research.

[20]  T. Ritz,et al.  Two Different Types of Light-Dependent Responses to Magnetic Fields in Birds , 2005, Current Biology.

[21]  K. Schulten,et al.  A perturbation treatment of oscillating magnetic fields in the radical pair mechanism using the Liouville equation , 1995 .

[22]  Thorsten Ritz,et al.  Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field , 2005, Naturwissenschaften.

[23]  W. Wiltschko,et al.  Light-dependent magnetoreception in birds: analysis of the behaviour under red light after pre-exposure to red light , 2004, Journal of Experimental Biology.

[24]  T. Fransson,et al.  Fuelling decisions in migratory birds: geomagnetic cues override the seasonal effect , 2007, Proceedings of the Royal Society B: Biological Sciences.

[25]  R. Haque,et al.  Dual regulation of cryptochrome 1 mRNA expression in chicken retina by light and circadian oscillators , 2002, Neuroreport.

[26]  W. Wiltschko,et al.  Light-dependent magnetoreception in birds: the effect of intensity of 565-nm green light , 2000, Naturwissenschaften.

[27]  Onur Güntürkün,et al.  Lateralization of magnetic compass orientation in a migratory bird , 2002, Nature.

[28]  S. Åkesson,et al.  Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light. , 2002, The Journal of experimental biology.

[29]  M. Davison,et al.  Magnetoreception and its trigeminal mediation in the homing pigeon , 2004, Nature.

[30]  J. Wild,et al.  Trigeminally innervated iron-containing structures in the beak of homing pigeons, and other birds , 2001, Brain Research.

[31]  Michael Winklhofer,et al.  Magnetite-based magnetoreception: the effect of repeated pulsing on the orientation of migratory birds , 2007, Journal of Comparative Physiology A.

[32]  Joseph L. Kirschvink,et al.  Magnetite biomineralization and magnetoreception in organisms , 1985 .

[33]  Aziz Sancar,et al.  Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. , 2003, Chemical reviews.

[34]  Beason,et al.  Does the avian ophthalmic nerve carry magnetic navigational information? , 1996, The Journal of experimental biology.

[35]  Baldissera Giovani,et al.  Light-induced electron transfer in a cryptochrome blue-light photoreceptor , 2003, Nature Structural Biology.

[36]  C. Demaine,et al.  Neurophysiological properties of magnetic cells in the pigeon's visual system , 1986, Journal of Comparative Physiology A.

[37]  W. Wiltschko,et al.  Disorientation of inexperienced young pigeons after transportation in total darkness , 1981, Nature.

[38]  Thorsten Ritz,et al.  Resonance effects indicate a radical-pair mechanism for avian magnetic compass , 2004, Nature.

[39]  Stephen T. Emlen,et al.  A TECHNIQUE FOR RECORDING MIGRATORY ORIENTATION OF CAPTIVE BIRDS , 1966 .

[40]  Michael Winklhofer,et al.  Superparamagnetic Magnetite in the Upper Beak Tissue of Homing Pigeons , 2000, Biometals.

[41]  O. Güntürkün Morphological asymmetries of the tectum opticum in the pigeon , 1997, Experimental Brain Research.

[42]  Bernd Schierwater,et al.  Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass , 2004, Naturwissenschaften.

[43]  T. Ritz,et al.  Magnetoreception in birds: Different physical processes for two types of directional responses , 2007, HFSP journal.

[44]  J. L. Gould,et al.  Biogenic magnetite as a basis for magnetic field detection in animals. , 1981, Bio Systems.

[45]  Durward D. Skiles,et al.  The Geomagnetic Field Its Nature, History, and Biological Relevance , 1985 .

[46]  W. Keeton,et al.  Magnets interfere with pigeon homing. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[47]  O. Güntürkün,et al.  Visual lateralization and homing in pigeons , 2004, Behavioural Brain Research.

[48]  N. Troje,et al.  Lateralized activation of Cluster N in the brains of migratory songbirds , 2007, The European journal of neuroscience.

[49]  W. Wiltschko,et al.  Bird navigation: what type of information does the magnetite-based receptor provide? , 2006, Proceedings of the Royal Society B: Biological Sciences.

[50]  K. Schulten,et al.  A model for photoreceptor-based magnetoreception in birds. , 2000, Biophysical journal.

[51]  R. Blakemore,et al.  Magnetotactic bacteria , 1975, Science.

[52]  R. Beason,et al.  Responses to small magnetic variations by the trigeminal system of the bobolink , 1990, Brain Research Bulletin.

[53]  J. K. Mai,et al.  Pattern of brain glucose utilization following magnetic stimulation. , 1990, Journal fur Hirnforschung.

[54]  Robert C. Beason,et al.  PIGEON HOMING: EFFECTS OF MAGNETIC PULSES ON INITIAL ORIENTATION , 1997 .

[55]  W. Wiltschko,et al.  Evidence for the use of magnetic outward-journey information in homing pigeons , 1978, Naturwissenschaften.

[56]  W. Wiltschko,et al.  Light-dependent magnetoreception in birds: the behaviour of European robins, Erithacus rubecula, under monochromatic light of various wavelengths and intensities. , 2001, The Journal of experimental biology.

[57]  W. Wiltschko Further Analysis of the Magnetic Compass of Migratory Birds , 1978 .

[58]  W. Wiltschko,et al.  A magnetic pulse leads to a temporary deflection in the orientation of migratory birds , 1994, Experientia.

[59]  J. Lind,et al.  Bird migration: Magnetic cues trigger extensive refuelling , 2001, Nature.

[60]  E D Yorke,et al.  A possible magnetic transducer in birds. , 1979, Journal of theoretical biology.

[61]  A. Davila,et al.  A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite , 2003 .

[62]  A. Sancar Structure and function of DNA photolyase. , 1994, Biochemistry.

[63]  R. Beason,et al.  Magnetic orientation and magnetically sensitive material in a transequatorial migratory bird , 1984, Nature.

[64]  Henrik Mouritsen,et al.  Night-vision brain area in migratory songbirds. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[65]  W. Wiltschko,et al.  The effect of yellow and blue light on magnetic compass orientation in European robins, Erithacus rubecula , 1999, Journal of Comparative Physiology A.

[66]  K. Schmidt-Koenig,et al.  Animal Migration, Navigation, and Homing , 1978 .

[67]  Paul Galland,et al.  Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana , 2007, Planta.

[68]  D Penny,et al.  Mass Survival of Birds Across the Cretaceous- Tertiary Boundary: Molecular Evidence , 1997, Science.

[69]  Beason,et al.  Behavioural evidence for the use of magnetic material in magnetoreception by a migratory bird , 1995, The Journal of experimental biology.

[70]  C. Walcott,et al.  Anomalies in the Earth’s Magnetic Field Increase the Scatter of Pigeons’ Vanishing Bearings , 1978 .

[71]  Wiltschko,et al.  Effect of a magnetic pulse on the orientation of silvereyes, zosterops l. lateralis, during spring migration , 1998, The Journal of experimental biology.

[72]  Wolfgang Wiltschko,et al.  Red light disrupts magnetic orientation of migratory birds , 1993, Nature.

[73]  Henrik Mouritsen,et al.  Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[74]  W. Keeton,et al.  Normal fluctuations in the earth's magnetic field influence pigeon orientation , 1974, Journal of comparative physiology.

[75]  W. Wiltschko,et al.  Lateralisation of magnetic compass orientation in silvereyes, Zosterops lateralis , 2003 .

[76]  Klaus Schulten,et al.  Magnetic Field Effects in Chemistry and Biology , 1982 .

[77]  D. Edmonds,et al.  A sensitive optically detected magnetic compass for animals , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[78]  E. Visalberghi,et al.  MAGNETIC INFLUENCES ON PIGEON HOMING , 1979 .

[79]  W. Wiltschko,et al.  Magnetic inclination compass: A basis for the migratory orientation of birds in the Northern and Southern Hemisphere , 1993, Experientia.

[80]  G. Falkenberg,et al.  A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons , 2007, Naturwissenschaften.

[81]  R. Robin Baker,et al.  Human Navigation and Magnetoreception , 1989 .

[82]  W. Wiltschko,et al.  Homing pigeons (Columba livia f. domestica) can use magnetic cues for locating food , 2007, Naturwissenschaften.

[83]  R. Wiltschko,et al.  Evidence for a Magnetite-Based Navigational “Map” in Birds , 1997, Naturwissenschaften.

[84]  Klaus Schulten,et al.  A perturbation theory treatment of oscillating magnetic fields in the radical pair mechanism , 1994 .

[85]  C. Walcott,et al.  Orientation of Homing Pigeons Altered by a Change in the Direction of an Applied Magnetic Field , 1974, Science.

[86]  W. Wiltschko,et al.  Pigeon Homing: Effect of Various Wavelengths of Light During Displacement , 1998, Naturwissenschaften.