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

Journal of Theoretical Biology

Volumn 262, Issue 1, 2010, Pages 129-141

  Jensen, Kenneth Kragh ^a,b  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Light dependent orientation responses; Magnetite; Magnetoreception; Monochromatic light; Radical pair mechanism

Indexed keywords

MAGNETITE;

BEHAVIORAL RESPONSE; COLOR; ECOLOGICAL MODELING; IRRADIANCE; LIGHT EFFECT; MAGNETITE; ORIENTATION BEHAVIOR; VISION; WAVELENGTH;

ARTICLE; ASSOCIATION; COLOR VISION; LIGHT; LIGHT IRRADIANCE; MAGNET; MATHEMATICAL MODEL; ORIENTING RESPONSE; PRIORITY JOURNAL; ADAPTATION; ANIMAL; BEHAVIOR; BIOLOGICAL MODEL; BIRD; EVALUATION; MAGNETISM; ORIENTATION; PHOTORECEPTOR CELL; PHOTOSTIMULATION; PHYSIOLOGY; POPULATION MIGRATION;

ANIMALIA; AVES;

ADAPTATION, BIOLOGICAL; ANIMAL MIGRATION; ANIMALS; BIRDS; CUES; LIGHT; MAGNETICS; MODELS, BIOLOGICAL; ORIENTATION; PHOTIC STIMULATION; PHOTORECEPTOR CELLS, VERTEBRATE; SPATIAL BEHAVIOR;

EID: 76449112858     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2009.09.005     Document Type: Article

References (94)

1. Able K.P. Common themes and variations in animal orientation systems. Am. Zool. 1991, 31:157-167.
2. Adair R.K. Effects of very weak magnetic fields on radical pair reformation. Bioelectromagnetics 1999, 20:255-263.
3. Batschelet E. Circular Statistics in Biology 1981, Academic Press, London.
4. Beason R.C., Nichols J.E. Magnetic orientation and magnetically sensitive material in a transequatorial migratory bird. Nature 1984, 309:151-153.
5. Bernard G.D., Wehner R. Functional similarities between polarization vision and color vision. Vis. Res. 1977, 17:1019-1028.
6. Cameron D.A., Easter S.S. The cone photoreceptor mosaic of the green sunfish (Leomis cyanellus). Visual Neurosci. 1993, 10:375-384.
7. Cintolesi F., Ritz T., Kay C.W.M., Timmel C.R., Hore P.J. Anisotropic recombination of an immobilized photoinduced radical pair in a 50μT magnetic field: a model avian photomagnetoreceptor. Chem. Phys. 2003, 294:385-399.
8. Coemans, M.A.J.M., Vos, J., 1992. On the perception of polarized light by the homing pigeon, Biological faculty, University of Utrecht, pp. 1-190.
9. Coemans M.A.J.M., Hzn J.J.V., Nuboer J.F.W. The relationship between celestial color gradients and the position of the sun with regard to the sun compass. Vis. Res. 1994, 34:1461-1470.
10. Coughlin D.J., Hawryshyn C.W. A cellular basis for polarized light vision in rainbow trout. J. Comp. Physiol. A 1995, 176:261-272.
11. Davila A.F., Fleissner G., Winklhofer M., Petersen N. A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite. Phys. Chem. Earth 2003, 28:647-652.
12. Davila A.F., Winklhofer M., Shcherbakov V.P., Petersen N. Magnetic pulse affects a putative magnetoreceptor mechanism. Biophys. J. 2005, 89:56-63.
13. Deutschlander M.E., Phillips J.B., Borland S.C. The case for light-dependent magnetic orientation in animals. J. Exp. Biol. 1999, 202:891-908.
14. Diebel C.E., Proksch R., Green C.R., Neilson P., Walker M.M. Magnetite defines a vertebrate magnetoreceptor. Nature 2000, 406:299-302.
15. Edmonds D.T. A magnetite null detector as the migrating bird's compass. Proc. R. Soc. London B 1992, 249:27-31.
16. Efimova O., Hore P.J. Role of exchange and dipolar interactions in the radical pair model of the avian magnetic compass. Biophys. J. 2008, 94:1565-1574.
17. Flamarique I.N., Hawryshyn C.W. The common white sucker (Catostomus commersoni): a fish with ultraviolet sensitivity that lacks polarization sensitivity. J. Comp. Physiol. A 1998, 182:331-341.
18. Flamarique I.N., Browman H.I. Wavelength-dependent polarization orientation in Daphnia. J. Comp. Physiol. A 2000, 186:1073-1087.
19. Fleissner G., Stahl B., Thalau P., Falkenberg G., Fleissner G. A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons. Naturwissenschaften 2007, 94:631-642.
20. Fleissner G., Holtkamp-Rotzler E., Hanzlik M., Winklhofer M., Fleissner G., Petersen N., Wiltschko W. Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 2003, 458:350-360.
21. Freake M.J., Phillips J.B. Light-dependent shift in bullfrog tadpole magnetic compass orientation: evidence for a common magnetoreception mechanism in anuran and urodele amphibians. Ethology 2005, 111:241-254.
22. Golden R.M. Mathematical Methods for Neural Network Analysis and Design 1996, MIT Press.
23. Govardovskii V.I., Fyhrquist N., Reuter T., Kuzmin D.G., Donner K. In search of the visual pigment template. Visual Neurosci. 2000, 17:509-528.
24. Hanzlik M., Heunemann C., Holtkamp-Rotzler E., Winklhofer M., Petersen N., Fleissner G. Superparamagnetic magnetite in the upper beak tissue of homing pigeons. Biometals 2000, 13:325-331.
25. Hart N.S., Hunt D.M. Avian visual pigments: characteristics, spectral tuning, and evolution. Am. Nat. 2007, 169:S7-S26.
26. Hawryshyn C.W., McFarland W.N. Cone photoreceptor mechanisms and the detection of polarized light in fish. J. Comp. Physiol. A 1987, 160:459-465.
27. Johnsen S., Lohmann K.J. The physics and neurobiology of magnetoreception. Nat. Rev. Neurosci. 2005, 6:703-712.
28. Johnsen S., Lohmann K.J. Magnetoreception in animals. Phys. Today 2008, 61:29-35.
29. Johnsen S., Mattern E., Ritz T. Light-dependent magnetoreception: quantum catches and opponency mechanisms of possible photosensitive molecules. J. Exp. Biol. 2007, 210:3171-3178.
30. Kelber A., Thunell C., Arikawa K. Polarisation-dependent colour vision in Papilio butterflies. J. Exp. Biol. 2001, 204:2469-2480.
31. Kinoshita M., Pfeiffer K., Homberg U. Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria. J. Exp. Biol. 2007, 210:1350-1361.
32. Kirschvink J.L., Gould J.L. Biogenic magnetite as a basis for magnetic field detection in animals. Biosystems 1981, 13:181-201.
33. Kirschvink J.L., Walker M.M. Particle-size considerations for magnetite-based magnetoreceptors. Magnetite Biomineralization and Mangetoreception in Organisms: A New Biomagnetism 1985, vol. 1:243-254. Plenum Press, New York, London.
34. Maeda K., Henbest K.B., Cintolesi F., Kuprov I., Rodgers C.T., Liddell P.A., Gust D., Timmel C.R., Hore P.J. Chemical compass model of avian magnetoreception. Nature 2008, 453:387-391.
35. Mouritsen H. Redstarts, Phoenicurus phoenicurus, can orient in a true-zero magnetic field. Anim. Behav. 1998, 55:1311-1324.
36. Muheim R. Magnetic compass calibration: a single calibration reference derived from sunset/sunrise polarized light cues from the region of sky near the horizon?. J. Ornithol. 2006, 147:50.
37. Muheim R., Backman J., Akesson S. Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light. J. Exp. Biol. 2002, 205:3845-3856.
38. Muheim, R., Bäckman, J., Åkesson, S., 2002b. Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light, Bird Orientation: External Cues and Ecological Factors, Lund University, 162pp.
39. Munro U., Munro J.A., Phillips J.B., Wiltschko W. Effect of wavelength of light and pulse magnetisation on different magnetoreception systems in a migratory bird. Austr. J. Zool. 1997, 45:189-198.
40. Parkyn D.C., Hawryshyn C.W. Polarized light sensitivity in rainbow trout (Oncorhyncus mukiss)-characterization from multiunit responses in the optic nerve. J. Comp. Physiol. A 1993, 172:493-500.
41. Phillips J.B., Borland S.C. Behavioural evidence for use of a light-dependent magnetoreception mechanism by a vertebrate. Nature 1992, 359:142-144.
42. Phillips J.B., Borland S.C. Wavelength specific effects of light on magnetic compass orientation of the eastern red-spotted newt Notophthalmus viridescens Ethol. Ecol. Evol. 1992, 4:33-42.
43. Phillips J.B., Sayeed O. Wavelength-dependent effects of light on magnetic compass orientation in Drosophila melanogaster. J. Comp. Physiol. A 1993, 172:303-308.
44. Ramsden S.D., Anderson L., Mussi M., Kamermans M., Hawryshyn C.W. Retinal processing and opponent mechanisms mediating ultraviolet polarization sensitivity in rainbow trout (Onchorhynchus mykiss). J. Exp. Biol. 2008, 211:1376-1385.
45. Rappl R., Wiltschko R., Weindler P., Berthold P., Wiltschko W. Orientation behavior of Garden Warblers (Sylvia borin) under monochromatic light of various wavelengths. Auk 2000, 117:256-260.
46. Ritz T., Adem S., Schulten K. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 2000, 78:707-718.
47. Rodgers C.T., Hore P.J. Chemical magnetoreception in birds: the radical pair mechanism. PNAS 2009, 106:353-360.
48. Rossel S., Wehner R. Celestial orientation in bees-the use of spectral cues. J. Comp. Physiol. A 1984, 155:605-613.
49. Sancar A. Cryptochromes as circadian photoreceptors in man and mouse. Photochem. Photobiol. 1999, 69:5S.
50. Sancar A. Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 2003, 103:2203-2237.
51. Schulten K. Magnetic field effects in chemistry and biology. Festkörperprobleme 1982, XXII:61-83.
52. Schulten K., Windemuth A., Maret G. Model for a physiological magnetic compass. Biophysical Effects of Steady Magnetic Fields 1986, 99-106. Springer, Berlin, Heidelberg, New York, London, Paris, Tokyo. N. Boccara (Ed.).
53. Shcherbakov V.P., Winklhofer M. The osmotic magnetometer: a new model for magnetite-based magnetoreceptors in animals. Eur. Biophys. J. Biophys. 1999, 28:380-392.
54. Solov'yov I.A., Greiner W. Theoretical analysis of an iron mineral-based magnetoreceptor model in birds. Biophys. J. 2007, 93:1493-1509.
55. Solov'yov I.A., Greiner W. Iron-mineral-based magnetoreceptor in birds: polarity or inclination compass?. Eur. Phys. J. D 2008, 51:161-172.
56. Solov'yov I.A., Schulten K. Magnetoreception through cryptochrome may involve superoxide. Biophys. J. 2009, 96:4804-4813.
57. Solov'yov I.A., Chandler D.E., Schulten K. Magnetic field effects in Arabidopsis thaliana cryptochrome-1. Biophys. J. 2007, 92:2711-2726.
58. Vacha M., Puzova T., Drstkova D. Effect of light wavelength spectrum on magnetic compass orientation in Tenebrio molitor. J. Comp. Physiol. A 2008, 194:853-859.
59. Walker M.M. A model for encoding of magnetic field intensity by magnetite-based magnetoreceptor cells. J. Theor. Biol. 2008, 250:85-91.
60. Walker M.M., Diebel C.E., Haugh C.V., Pankhurst P.M., Montgomery J.C., Green C.R. Structure and function of the vertbrate magnetic sense. Nature 1997, 390:371-376.
61. Wang K., Mattern E., Ritz T. On the use of magnets to disrupt the physiological compass of birds. Phys. Biol. 2006, 3:220-231.
62. Weaver J.C., Vaughan T.E., Astumian R.D. Biological sensing of small field differences by magnetically sensitive chemical reactions. Nature 2000, 405:707-709.
63. Wehner R. The perception of polarised light. The Biology of Photo Reception 1983, Cambridge University Press, Cambridge. D.J. Cosens, D. Vince-Prue (Eds.).
64. Wehner R. The ant's celestial compass system: spectral and polarization channels. Orientation and Communication in Arthropods 1997, 145-185. Birkhäuser, Basel. M. Lehrer (Ed.).
65. Wehner R., Bernard G.D., Geiger E. Twisted and non-twisted rhabdoms and their significance for polarization detection in the bee. J. Comp. Physiol. A 1975, 104:225-245.
66. Williams M.N., Wild J.M. Trigeminally innervated iron-containing structures in the beak of homing pigeons, and other birds. Brain Res. 2001, 889:243-246.
67. Wiltschko R., Wiltschko W. Magnetic Orientation in Animals 1995, Springer, Berlin.
68. Wiltschko R., Wiltschko W. Pigeon homing: effect of various wavelengths of light during displacement. Naturwissenschaften 1998, 85:164-167.
69. Wiltschko R., Wiltschko W. The orientation system of birds-I. Compass mechanisms. J. Ornithol. 1999, 140:1-40.
70. Wiltschko R., Wiltschko W. Magnetoreception. Bioessays 2006, 28:157-168.
71. Wiltschko R., Wiltschko W., Davies M.N.O., Green P.R. Avian orientation: Multiple Sensory Cues and the Advantage of Redundancy, Perception and Motor Control in Birds 1994, Springer, Berlin, Heidelberg, pp. 95-119.
72. Wiltschko R., Stapput K., Bischof H.J., Wiltschko W. Light-dependent magnetoreception in birds: increasing intensity of monochromatic light changes the nature of the response. Front. Zool. 2007, 4:1. 10.1186/1742-9994-4-5.
73. Wiltschko R., Ritz T., Stapput K., Thalau P., Wiltschko W. Two different types of light-dependent responses to magnetic fields in birds. Curr. Biol. 2005, 15:1518-1523.
74. Wiltschko R., Munro U., Ford H., Stapput K., Wiltschko W. Light-dependent magnetoreception: orientation behaviour of migratory birds under dim red light. J. Exp. Biol. 2008, 211:3344-3350.
75. Wiltschko W. The influence of magnetic total intensity and inclination on directions preferred by migrating European robins (Erithacus rubecula). Animal Orientation and Navigation 1972, 569-578. NASA SP, Washington, DC. S.R. Galler (Ed.).
76. Wiltschko W., Wiltschko R. Navigation in birds and other animals. J. Nav. 1993, 46:174-191.
77. Wiltschko W., Wiltschko R. Migratory orientation of European robins is affected by the wavelength as well as by a magnetic pulse. J. Comp. Physiol. A 1995, 177:363-369.
78. Wiltschko W., Wiltschko R. The effect of yellow and blue light on magnetic compass orientation in European robins, Erithacus rubecula. J. Comp. Physiol. A 1999, 184:295-299.
79. Wiltschko W., Wiltschko R. Light-dependent magnetoreception in birds: does directional information change with light intensity?. Naturwissenschaften 2000, 87:36-40.
80. Wiltschko W., Wiltschko R. Light-dependent magnetoreception in birds: the behaviour of European robins, Erithacus rubecula, under monochromatic light of various wavelengths and intensities. J. Exp. Biol. 2001, 204:3295-3302.
81. Wiltschko W., Wiltschko R. Magnetic compass orientation in birds and its physiological basis. Naturwissenschaften 2002, 89:445-452.
82. Wiltschko W., Wiltschko R. Magnetic orientation and magnetoreception in birds and other animals. J. Comp. Physiol. A 2005, 191:675-693.
83. Wiltschko W., Wiltschko R., Munro U. Light dependent magnetoreception in birds: the effect of intensity of 565nm green light. Naturwissenschaften 2000, 87:366-369.
84. Wiltschko W., Gesson M., Wiltschko R. Magnetic compass orientation of European robins under 565nm green light. Naturwissenschaften 2001, 88:387-390.
85. Wiltschko W., Munro U., Ford H., Wiltschko R. Red light disrupts magnetic orientation of migratory birds. Nature 1993, 364:525-527.
86. Wiltschko W., Munro U., Ford H., Wiltschko R. Magnetic orientation in birds: non-compass responses under monochromatic light of increased intensity. Proc. R. Soc. London B 2003, 270:2133-2140.
87. Wiltschko W., Gesson M., Stapput K., Wiltschko R. Light-dependent magnetoreception in birds: interaction of at least two different receptors. Naturwissenschaften 2004, 91:130-134.
88. Wiltschko W., Moller A., Gesson M., Noll C., Wiltschko R. Light-dependent magnetoreception in birds: analysis of the behaviour under red light after pre-exposure to red light. J. Exp. Biol. 2004, 207:1193-1202.
89. Wiltschko W., Freire R., Munro U., Ritz T., Rogers L., Thalau P., Wiltschko R. The magnetic compass of domestic chickens, Gallus gallus. J. Exp. Biol. 2007, 210:2300-2310.
90. Winklhofer M., Holtkamp-Rotzler E., Hanzlik M., Fleissner G., Petersen N. Clusters of superparamagnetic magnetite particles in the upper-beak skin of homing pigeons: evidence of a magnetoreceptor?. Eur. J. Mineral. 2001, 13:659-669.
91. Yorke E.D. A possible magnetic transducer in birds. J. Theor. Biol. 1979, 77:101-105.
92. Yorke E.D. Sensivity of pigeons to small magnetic field variations. J. Theor. Biol. 1981, 89:533-537.
93. Yorke E.D., Kirschvink J.L., Jones D.S., MacFadden B.J. Energetics and sensivity considerations of ferromagnetic magnetoreceptors. Magnetite Biomineralization and Mangetoreception in Organisms: A New Biomagnetism 1985, vol. 1:233-242. Plenum Press, New York, London.
94. Zar J.H. Biostatistical Analysis 1996, Prentice-Hall, Upper Saddle River, NJ, USA.