Orientation of Birds in Total Darkness

Magnetic compass orientation of migratory birds is known to be light dependent, and radical-pair processes have been identified as the underlying mechanism. Here we report for the first time results of tests with European robins, Erithacus rubecula, in total darkness and, as a control, under 565 nm green light. Under green light, the robins oriented in their normal migratory direction, with southerly headings in autumn and northerly headings in spring. By contrast, in darkness they significantly preferred westerly directions in spring as well as autumn. This failure to show the normal seasonal change characterizes the orientation in total darkness as a "fixed direction" response. Tests in magnetic fields with the vertical or the horizontal component inverted showed that the preferred direction depended on the magnetic field but did not involve the avian inclination compass. A high-frequency field of 1.315 MHz did not affect the behavior, whereas local anesthesia of the upper beak resulted in disorientation. The behavior in darkness is thus fundamentally different from normal compass orientation and relies on another source of magnetic information: It does not involve the radical-pair mechanism but rather originates in the iron-containing receptors in the upper beak.

[1]  K. Lohmann Magnetic orientation by hatchling loggerhead sea turtles (Caretta caretta). , 1991, The Journal of experimental biology.

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

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

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

[5]  J. Kirschvink,et al.  'Fixed-axis' magnetic orientation by an amphibian: non-shoreward-directed compass orientation, misdirected homing or positioning a magnetite-based map detector in a consistent alignment relative to the magnetic field? , 2002, The Journal of experimental biology.

[6]  J. L. Gould,et al.  Pigeons have magnets. , 1979, Science.

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

[8]  S. Begall,et al.  Magnetic compass in the cornea: local anaesthesia impairs orientation in a mammal , 2006, Journal of Experimental Biology.

[9]  P. Schlegel Spontaneous preferences for magnetic compass direction in the American red-spotted newt, Notophthalmus viridescens (Salamandridae, Urodela) , 2007, Journal of Ethology.

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

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

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

[13]  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.

[14]  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.

[15]  E. L. Brannon,et al.  The use of celestial and magnetic cues by orienting sockeye salmon smolts , 1982, Journal of comparative physiology.

[16]  T. Quinn Evidence for celestial and magnetic compass orientation in lake migrating sockeye salmon fry , 1980, Journal of comparative physiology.

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

[18]  Wolfgang Wiltschko,et al.  Magnetoreception in birds: two receptors for two different tasks , 2007, Journal of Ornithology.

[19]  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.

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

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

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

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

[24]  R. Beason You Can Get There from Here: Responses to Simulated Magnetic Equator Crossing by the Bobolink (Dolichonyx oryzivorus) , 2010 .

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

[26]  K. Lohmann,et al.  Disruption of magnetic orientation in hatchling loggerhead sea turtles by pulsed magnetic fields , 2005, Journal of Comparative Physiology A.

[27]  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.

[28]  E. Gwinner Endogenous temporal control of migratory restlessness in warblers , 1974, Naturwissenschaften.

[29]  W. Wiltschko,et al.  A Magnetic Polarity Compass for Direction Finding in a Subterranean Mammal , 1997, Naturwissenschaften.

[30]  Hynek Burda,et al.  The magnetic compass mechanisms of birds and rodents are based on different physical principles , 2006, Journal of The Royal Society Interface.

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

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

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

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

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

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

[37]  J. Phillips,et al.  Magnetic compass orientation is eliminated under near-infrared light in the eastern red-spotted newt Notophthalmus viridescens , 1992, Animal Behaviour.

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

[39]  K. Lohmann,et al.  A Light-Independent Magnetic Compass in the Leatherback Sea Turtle. , 1993, The Biological bulletin.

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

[41]  K. Lohmann,et al.  GEOMAGNETIC ORIENTATION OF LOGGERHEAD SEA TURTLES: EVIDENCE FOR AN INCLINATION COMPASS , 1993 .

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

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

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

[45]  Borland,et al.  Ferromagnetic material in the eastern red-spotted newt notophthalmus viridescens , 1999, The Journal of experimental biology.

[46]  Stuart Parsons,et al.  Bats respond to polarity of a magnetic field , 2007, Proceedings of the Royal Society B: Biological Sciences.