Light-dependent orientation responses in animals can be explained by a model of compass cue integration.

The magnetic compass sense of animals is currently thought to be based on light-dependent processes like the proposed radical pair mechanism. In accordance, many animals show orientation responses that depend on light. However, the orientation responses depend on the wavelength and irradiance of monochromatic light in rather complex ways that cannot be explained directly by the radical pair mechanism. Here, a radically different model is presented that can explain a vast majority of the complex observed light-dependent responses. The model put forward an integration process consisting of simple lateral inhibition between a normal functioning, light-independent magnetic compass (e.g. magnetite based) and a vision based skylight color gradient compass that misperceives compass cues in monochromatic light. Integration of the misperceived color compass cue and the normal magnetic compass not only explains most of the categorically different light-dependent orientation responses, but also shows a surprisingly good fit to how well the animals are oriented (r-values) under light of different wavelength and irradiance. The model parsimoniously suggests the existence of a single magnetic sense in birds (probably based on magnetic crystals).

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

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

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

[4]  W. Wiltschko,et al.  Migratory orientation of European Robins is affected by the wavelength of light as well as by a magnetic pulse , 1995, Journal of Comparative Physiology A.

[5]  John C. Montgomery,et al.  Structure and function of the vertebrate magnetic sense , 1997, Nature.

[6]  H. Browman,et al.  Wavelength-dependent polarization orientation in Daphnia , 2000, Journal of Comparative Physiology A.

[7]  W. Wiltschko,et al.  Light-Dependent Magnetoreception in Birds: Does Directional Information Change with Light Intensity? , 2000, Naturwissenschaften.

[8]  T. Ritz,et al.  Light-dependent magnetoreception: quantum catches and opponency mechanisms of possible photosensitive molecules , 2007, Journal of Experimental Biology.

[9]  J. Kirschvink,et al.  Magnetite biomineralization and magnetoreception in organisms : a new biomagnetism , 1985 .

[10]  W. Wiltschko,et al.  Magnetic compass orientation of European robins under 565 nm green light , 2001, Naturwissenschaften.

[11]  W. Wiltschko,et al.  Navigation in Birds and Other Animals , 1993, Journal of Navigation.

[12]  W. Greiner,et al.  Iron-mineral-based magnetoreceptor in birds: polarity or inclination compass? , 2009 .

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

[14]  K. Donner,et al.  In search of the visual pigment template , 2000, Visual Neuroscience.

[15]  C. Hawryshyn,et al.  The common white sucker (Catostomus commersoni ): a fish with ultraviolet sensitivity that lacks polarization sensitivity , 1998, Journal of Comparative Physiology A.

[16]  C.,et al.  Polarisation-dependent colour vision in Papilio butterflies POLARISATION-DEPENDENT COLOUR VISION IN PAPILIO BUTTERFLIES , 2001 .

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

[18]  Ilya Kuprov,et al.  Chemical compass model of avian magnetoreception , 2008, Nature.

[19]  K. Schulten,et al.  Model for a physiological magnetic compass , 1986 .

[20]  D. Hunt,et al.  Avian Visual Pigments: Characteristics, Spectral Tuning, and Evolution , 2007, The American Naturalist.

[21]  Sönke Johnsen,et al.  Magnetoreception in animals , 2008 .

[22]  M. Vacha,et al.  Effect of light wavelength spectrum on magnetic compass orientation in Tenebrio molitor , 2008, Journal of Comparative Physiology A.

[23]  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.

[24]  R. Wehner The ant’s celestial compass system: spectral and polarization channels , 1997 .

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

[26]  R. Wehner,et al.  Celestial orientation in bees: the use of spectral cues , 1984, Journal of Comparative Physiology A.

[27]  W. Greiner,et al.  Theoretical analysis of an iron mineral-based magnetoreceptor model in birds. , 2007, Biophysical journal.

[28]  Nino Boccara,et al.  Biophysical Effects of Steady Magnetic Fields , 1986 .

[29]  M. A. Coemans,et al.  The relation between celestial colour gradients and the position of the sun, with regard to the sun compass , 1994, Vision Research.

[30]  D. Edmonds A magnetite null detector as the migrating bird’s compass , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

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

[33]  E. Yorke,et al.  Energetics and Sensitivity Considerations of Ferromagnetic Magnetoreceptors , 1985 .

[34]  Thorsten Ritz,et al.  Anisotropic recombination of an immobilized photoinduced radical pair in a 50-μT magnetic field: a model avian photomagnetoreceptor , 2003 .

[35]  M. Lehrer Orientation and Communication in Arthropods , 1997, EXS.

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

[37]  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.

[38]  Michael Winklhofer,et al.  Clusters of superparamagnetic magnetite particles in the upper-beak skin of homing pigeons evidence of a magnetoreceptor? , 2001 .

[39]  M. Vences,et al.  Evidence for recent gene flow between north-eastern and south-eastern Madagascan poison frogs from a phylogeography of the Mantella cowani group , 2007, Frontiers in Zoology.

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

[41]  W. Wiltschko The influence of magnetic total intensity and inclination on directions preferred by migrating European robins (Erithacus rubecula) , 1972 .

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

[43]  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.

[44]  A. Kelber,et al.  Polarisation-dependent colour vision in Papilio butterflies. , 2001, The Journal of experimental biology.

[45]  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.

[46]  S. Chris Borland,et al.  Behavioural evidence for use of a light-dependent magnetoreception mechanism by a vertebrate , 1992, Nature.

[47]  P. Hore,et al.  Role of exchange and dipolar interactions in the radical pair model of the avian magnetic compass. , 2008, Biophysical journal.

[48]  R. Astumian,et al.  Biological sensing of small field differences by magnetically sensitive chemical reactions , 2000, Nature.

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

[50]  Sönke Johnsen,et al.  The physics and neurobiology of magnetoreception , 2005, Nature Reviews Neuroscience.

[51]  Klaus Schulten,et al.  Magnetoreception through cryptochrome may involve superoxide. , 2009, Biophysical journal.

[52]  K. Able Magnetic orientation and magnetoreception in birds , 1994, Progress in Neurobiology.

[53]  G. D. Bernard,et al.  Functional similarities between polarization vision and color vision , 1977, Vision Research.

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

[55]  Klaus Schmidt-Koenig,et al.  Animal Orientation and Navigation , 1972 .

[56]  E. Yorke Sensitivity of pigeons to small magnetic field variations. , 1981, Journal of theoretical biology.

[57]  J. Phillips,et al.  Light‐Dependent Shift in Bullfrog Tadpole Magnetic Compass Orientation: Evidence for a Common Magnetoreception Mechanism in Anuran and Urodele Amphibians , 2005 .

[58]  Richard M. Golden,et al.  Mathematical Methods for Neural Network Analysis and Design , 1996 .

[59]  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.

[60]  R. Beason Magnetic Orientation and Magnetically Sensitive Material in Migratory Birds , 1986 .

[61]  Borland,et al.  The case for light-dependent magnetic orientation in animals , 1999, The Journal of experimental biology.

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

[63]  E. Batschelet Circular statistics in biology , 1981 .

[64]  T. Ritz,et al.  On the use of magnets to disrupt the physiological compass of birds , 2006, Physical biology.

[65]  C. Hawryshyn,et al.  A cellular basis for polarized-light vision in rainbow trout , 1995, Journal of Comparative Physiology A.

[66]  C. Hawryshyn,et al.  Polarized-light sensitivity in rainbow trout (Oncorhynchus mykiss): characterization from multi-unit responses in the optic nerve , 1993, Journal of Comparative Physiology A.

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

[68]  K. Lohmann Magnetic compass orientation , 1993, Nature.

[69]  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.

[70]  R. Adair Effects of very weak magnetic fields on radical pair reformation. , 1999, Bioelectromagnetics.

[71]  S. Easter,et al.  The cone photoreceptor mosaic of the green sunfish, Lepomis cyanellus , 1993, Visual Neuroscience.

[72]  J. Phillips,et al.  Wavelength specific effects of light on magnetic compass orientation of the eastern red-spotted newt Notophthalmus viridescens , 1992 .

[73]  Kenneth P. Able,et al.  Common Themes and Variations in Animal Orientation Systems , 1991 .

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

[75]  Danielle E. Chandler,et al.  Magnetic field effects in Arabidopsis thaliana cryptochrome-1. , 2007, Biophysical journal.

[76]  R. Wiltschko,et al.  Das Orientierungssystem der Vögel I. Kompaßmechanismen , 2006, Journal für Ornithologie.

[77]  Alfonso F Davila,et al.  Magnetic pulse affects a putative magnetoreceptor mechanism. , 2005, Biophysical journal.

[78]  T. Ritz,et al.  The magnetic compass of domestic chickens, Gallus gallus , 2007, Journal of Experimental Biology.

[79]  O. Sayeed,et al.  Wavelength-dependent effects of light on magnetic compass orientation in Drosophila melanogaster , 1993, Journal of Comparative Physiology A.

[80]  C. Hawryshyn,et al.  Cone photoreceptor mechanisms and the detection of polarized light in fish , 1987, Journal of Comparative Physiology A.

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

[82]  W. Wiltschko,et al.  Light-dependent magnetoreception: orientation behaviour of migratory birds under dim red light , 2008, Journal of Experimental Biology.

[83]  P. Hore,et al.  Chemical magnetoreception in birds: The radical pair mechanism , 2009, Proceedings of the National Academy of Sciences.

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

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

[86]  M. Walker,et al.  A model for encoding of magnetic field intensity by magnetite-based magnetoreceptor cells. , 2008, Journal of theoretical biology.

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

[88]  U. Homberg,et al.  Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria , 2007, Journal of Experimental Biology.

[89]  H. Mouritsen Redstarts, Phoenicurus phoenicurus , can orient in a true-zero magnetic field , 1998, Animal Behaviour.

[90]  G. D. Bernard,et al.  Twisted and non-twisted rhabdoms and their significance for polarization detection in the bee , 1975, Journal of comparative physiology.

[91]  W. Wiltschko,et al.  Magnetic orientation and magnetoreception in birds and other animals , 2005, Journal of Comparative Physiology A.

[92]  W. Wiltschko,et al.  Effect of Wavelength of Light and Pulse Magnetisation on Different Magnetoreception Systems in a Migratory Bird , 1997 .

[93]  M. Kamermans,et al.  Retinal processing and opponent mechanisms mediating ultraviolet polarization sensitivity in rainbow trout (Oncorhynchus mykiss) , 2008, Journal of Experimental Biology.

[94]  Roger Proksch,et al.  Magnetite defines a vertebrate magnetoreceptor , 2000, Nature.