Biophysics of magnetic orientation: Strengthening the interface between theory and experimental design

Journal of the Royal Society Interface

Volumn 7, Issue SUPPL. 2, 2010, Pages

  Kirschvink, Joseph L ^a   Winklhofer, Michael ^b   Walker, Michael M ^c  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Animal navigation; Double blind protocols; Geomagnetism; Magnetite; Magnetoreception; Radical pairs

Indexed keywords

ANIMALS; BIOMAGNETISM; GEOMAGNETISM; MAGNETIC FIELD EFFECTS; MAGNETITE; NAVIGATION; RADIO BROADCASTING; RADIO TRANSMISSION; TRACKING (POSITION);

BIOCHEMICAL REACTIONS; BIOGENIC MAGNETITE; BIOPHYSICAL MECHANISM; CONTROL OF EXPERIMENTS; DATA CAPTURE; DOUBLE-BLIND PROTOCOLS; EXPERIMENTAL DESIGN; EXPERIMENTAL STUDIES; FIELD EXPERIMENT; LONG DISTANCES; MAGNETIC EFFECTS; MAGNETIC ORIENTATION; MAGNETORECEPTION; MAGNETORECEPTOR; MIGRATORY BIRDS; RADICAL PAIR; RADIO SIGNALS; REPRODUCIBILITIES; TECHNIQUES USED; TRACKING DEVICES;

EXPERIMENTS;

MAGNETITE;

BIOMAGNETISM; ELECTROMAGNETIC FIELD; MAGNETIC FIELD; MAGNETORECEPTION; MIGRANT BIRD; PHOTOACTIVATION; PHOTORECEPTOR POTENTIAL; RADIOFREQUENCY; REVIEW; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIOPHYSICS; BIRD; HUMAN; LIGHT; METHODOLOGY; ORIENTATION; PERCEPTION; PHYSIOLOGY; POPULATION MIGRATION; RADIATION EXPOSURE;

ANIMALIA; AVES; COLUMBA;

ANIMAL MIGRATION; ANIMALS; BIOPHYSICS; BIRDS; ELECTROMAGNETIC FIELDS; HUMANS; LIGHT; MODELS, BIOLOGICAL; ORIENTATION; PERCEPTION;

EID: 77950179632     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2009.0491.focus     Document Type: Review

References (94)

1. Adair, R. K. 1991 Constraints on biological effects of weak extremely-low frequency electromagnetic fields. Phys. Rev. A 43, 1039-1048. (doi:10.1103/PhysRevA.43.1039)
2. Ahmad, M., Galland, P., Ritz, T., Wiltschko, R. & Wiltschko, W. 2007 Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana. Planta 225, 615-624. (doi:10.1007/s00425-006-0383-0)
3. Bazylinski, D. A., Schlezinger, D. R., Howes, B. H., Frankel, R. B. & Epstein, S. S. 2000 Occurrence and distribution of diverse populations of magnetic protists in a chemically stratified coastal salt pond. Chem. Geol. 169, 319-328. (doi:10.1016/S0009-2541(00)00211-4)
4. Beason, R. C., Wiltschko, R. & Wiltschko, W. 1997 Pigeon homing: effects of magnetic pulses on initial orientation. Auk 114, 405-415.
5. Beaugrand, J. P. 1976 An attempt to confirm magnetic sensitivity in the pigeon, Columba livia. J. Comp. Phys. 110, 343-355. (doi:10.1007/BF00659150)
6. Blakemore, R. 1975 Magnetotactic bacteria. Science 190, 377-379. (doi:10.1126/science.170679)
7. Block, S. M. 1992 Biophysical aspects of sensory transduction. In Sensory transduction, vol. 45 (eds D. P. Corey & S. D. Roper), pp. 424. Woods Hole, MA: Marine Biological Laboratory, Rockfeller University Press.
8. Bookman, M. A. 1977 Sensitivity of the homing pigeon to an Earth-strength magnetic field. Nature 267, 340-342. (doi:10.1038/267340a0)
9. Brown, F. L. H. 2003 Regulation of protein mobility via thermal membrane undulations. Biophys. J. 84, 842-853. (doi:10.1016/S0006-3495(03)74903-0)
10. Carman, G. J., Walker, M. M. & Lee, A. K. 1987 Attempts to demonstrate magnetic discrimination by homing pigeons in flight. Anim. Learn. Behav. 15, 124-129.
11. Cross, A. J. & Fleming, G. R. 1986 Influence of inhibitor binding on the internal motions of lysozyme. Biophys. J. 50, 507-512. (doi:10.1016/S0006- 3495(86)83488-9)
12. Diebel, C. E., Proksch, R., Green, C. R., Neilson, P. &Walker, M. M. 2000 Magnetite defines a vertebrate magnetoreceptor. Nature 406, 299-302. (doi:10.1038/35018561)
13. Fischer, J. H., Freake, M. J., Borland, S. C. & Phillips, J. B. 2001 Evidence for the use of magnetic map information by an amphibian. Anim. Behav. 62, 1-10. (doi:10.1006/anbe.2000.1722)
14. Fleissner, G., Holtkamp-Rotzler, E., Hanzlik, M., Winklhofer, M., Petersen, N. & Wiltschko, W. 2003 Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 458, 350-360. (doi:10.1002/cne.10579)
15. Gellermann, L. W. 1933 Chance orders of alternating stimuli in visual discrimination experiments. J. Genet. Psychol. 42, 206-208.
16. Gould, S. J. & Vrba, E. S. 1982 Exaptation - a missing term in the science of form. Paleobiology 8, 4-15.
17. Griffin, D. R. 1944 The sensory basis of bird navigation. Q. Rev. Biol. 19, 15-31. (doi:10.1086/394685)
18. Griffin, D. R. 1969 Physiology and geophysics of bird navigation. Q. Rev. Biol. 44, 255-276. (doi:10.1086/406142)
19. Hanzlik, M., Heunemann, C., Holtkamp-Rotzler, E., Winklhofer, M., Petersen, N. & Fleissner, G. 2000 Superparamagnetic magnetite in the upper beak tissue of homing pigeons. Biometals 13, 325-331. (doi:10.1023/A: 1009214526685)
20. Harris, S.-R., Henbest, K. B., Maeda, K., Pannell, J. R., Timmel, C. R., Hore, P. J. & Okamoto, H. 2009 Effect of magnetic fields on cryptochrome-dependent responses in Arabidopsis thaliana. J. R. Soc. Interface 6, 1193-1205. (doi:10.1098/rsif.2008.0519)
21. Hill, E. & Ritz, T. 2010 Can disordered radical pair systems provide a basis for a magnetic compass in animals? J. R. Soc. Interface 7, S265-S271. (doi:10.1098/rsif.2009.0378.focus)
22. Holland, R. A., Kirschvink, J. L., Doak, T. G. & Wikelski, M. 2008 Bats use magnetite to detect the Earth's magnetic field. PLoS ONE 3, e1676-e1676. (doi:10.1371/journal.pone.0001676)
23. Howard, J. 2001 Mechanics of motor proteins and the cytoskeleton. Sunderland, MA: Sinauer.
24. Jeffery, G. B. 1922 The motion of ellipsoidal particles immersed in a viscous fluid. Proc. R. Soc. Lond. A 102, 161-179. (doi:10.1098/rspa.1922.0078)
25. Jensen, K. K. 2010 Light-dependent orientation responses in animals can be explained by a model of compass cue integration. J. Theor. Biol. 262, 129-141. (doi:10.1016/j.jtbi.2009.09.005)
26. Kalmijn, A. J. 1981 Biophysics of geomagnetic field detection. IEEE Trans. Magn. 17, 1113-1124. (doi:10.1109/TMAG.1981.1061156)
27. Kalmijn, A. J. & Blakemore, R. P. 1978 The magnetic behavior of mud bacteria. In Animal migration, navigation and homing (eds K. Schmidt-Koenig & W. T. Keeton), pp. 354-355. Berlin, Germany: Springer-Verlag.
28. Kirschvink, J. L. 1979 I. A paleomagnetic approach to the Precambrian-Cambrian boundary problem. II. Biogenic magnetite: its role in the magnetization of sediments and as the basis of magnetic field detection in animals. PhD thesis, Division of geological & geophysical sciences. Princeton, NJ: Princeton University.
29. Kirschvink, J. L. 1980 South-seeking magnetic bacteria. J. Exp. Biol. 86, 345-347.
30. Kirschvink, J. L. 1992a Constraints on biological effects of weak extremely low-frequency electromagnetic fields comment. Phys. Rev. A 46, 2178-2184. (doi:10.1103/PhysRevA.46.2178)
31. Kirschvink, J. L. 1992b Uniform magnetic fields and double-wrapped coil systems: improved techniques for the design of biomagentic experiments. Bioelectromagnetics 13, 401-411. (doi:10.1002/bem.2250130507)
32. Kirschvink, J. L. 1997 Magnetoreception: homing in on vertebrates. Nature 390, 339-340. (doi:10.1038/36986)
33. Kirschvink, J. L. & Gould, J. L. 1981 Biogenic magnetite as a basis for magnetic field sensitivity in animals. BioSystems 13, 181-201. (doi:10.1016/0303-2647(81)90060-5)
34. Kirschvink, J. L. & Hagadorn, J. W. 2000 A grand unified theory of biomineralization. In Biomineralization (ed. E. Bäuerlein), ch. 10, pp. 139-150. Weinheim, Germany: Wiley-VCH.
35. Kirschvink, J. L. & Kobayashi-Kirschvink, A. 1991 Is geomagnetic sensitivity real? Replication of the Walker-Bitterman conditioning experiment in honey bees. Am. Zool. 31, 169-185.
36. Kirschvink, J. L. & Walker, M. M. 1985 Particle-size considerations for magnetite-based magnetoreceptors. In Magnetite biomineralization and magnetoreception in organisms: a new biomagnetism, vol. 5 (eds J. L. Kirschvink, D. S. Jones & B. McFadden), pp. 243-254. New York, NY: Plenum Press.
37. Kirschvink, J. L., Jones, D. S. & McFadden, B. J. 1985a Magnetite biomineralization and magnetoreception in organisms: a new biomagnetism. Topics in geobiology. New York, NY: Plenum Press.
38. Kirschvink, J. L., Walker, M. M., Chang, S.-B. R., Dizon, A. E. & Peterson, K. A. 1985b Chains of single-domain magnetite particles in Chinook salmon (Oncorhynchus tshawytscha). J. Comp. Physiol. 157, 375-381. (doi:10.1007/BF00618127)
39. Kirschvink, J. L., Dizon, A. E. & Westphal, J. A. 1986 Evidence from strandings for geomagnetic sensitivity in Cetaceans. J. Exp. Biol. 120, 1-24.
40. Kirschvink, J. L., Padmanabha, S., Boyce, C. K. & Oglesby, J. 1997 Measurement of the threshold sensitivity of honeybees to weak, extremely low frequency magnetic fields. J. Exp. Biol. 200, 1363-1368.
41. Kirschvink, J. L., Walker, M. M. & Diebel, C. 2001 Magnetite-based magnetoreception. Curr. Opin. Neurobiol. 11, 462-467. (doi:10.1016/S0959- 4388(00)00235-X)
42. Klinowska, M. 1985 Cetacean live stranding sites relate to geomagnetic topography. Aquat. Mamm. 11, 27-32.
43. Kreithen, M. L. & Keeton,W. T. 1974 Detection of changes in atmospheric pressure by the homing pigeon, Columba livia. J. Comp. Physiol. 89, 73-82. (doi:10.1007/BF00696164)
44. Lau, J. C. S., Wagner-Rundell, N., Rodgers, C. T., Green, N. J. B. & Hore, P. J. 2010 Effects of disorder and motion in a radical pair magnetoreceptor. J. R. Soc. Interface 7, S257-S264. (doi:10.1098/rsif.2009.0399. focus)
45. Leonhardt, R. & Fabian, K. 2007 Paleomagnetic reconstruction of the global geomagnetic field evolution during the Matuyama/Brunhes transition: iterative Bayesian inversion and independent verification. Earth Planet. Sci. Lett. 253, 172-195. (doi:10.1016/j.epsl.2006.10.025)
46. Leonhardt, R., Fabian, K., Winklhofer, M., Ferk, A., Laj, C. & Kissel, C. 2009 Geomagnetic field evolution during the Laschamp excursion. Earth Planet. Sci. Lett. 278, 87-95. (doi:10.1016/j.epsl.2008.11.028)
47. Liedvogel, M. & Mouritsen, H. 2010 Cryptochromes - a potential magnetoreceptor: what do we know and what do we want to know? J. R. Soc. Interface 7, S147-S162. (doi:10.1098/rsif.2009.0411.focus)
48. Liedvogel, M., Maeda, K., Henbest, K., Schleicher, E., Simon, T., Timmel, C. R., Hore, P. J. & Mouritsen, H. 2007 Chemical magnetoreception: bird cryptochrome 1a is excited by blue light and forms long-lived radical-pairs. PLoS ONE 2, e1106. (doi:10.1371/journal.pone.0001106)
49. Lohmann, K. J., Pentcheff, N. D., Nevitt, G. A., Stetten, G. D., Zimmer-Faust, R. K., Jarrard, H. E. & Boles, L. C. 1995 Magnetic orientation of spiny lobsters in the ocean: experiments with undersea coil systems. J. Exp. Biol. 198, 2041-2048.
50. Lowenstam, H. A. 1962 Magnetite in denticle capping in recent chitons ( polyplacophora). Geol. Soc. Am. Bull. 73, 435-438. (doi:10.1130/0016-7606(1962) 73[435:MIDCIR]2.0.CO;2)
51. Maeda, K., Henbest, K. B., Cintolesi, F., Kuprov, I., Rodgers, C. T., Liddell, P. A., Gust, D., Timmel, C. R. & Hore, P. J. 2008 Chemical compass model of avian magnetoreception. Nature 453, 387-390. (doi:10.1038/nature06834)
52. Marhold, S., Wiltschko, W. & Burda, H. 1997 A magnetic polarity compass for direction finding in a subterranean mammal. Naturwissenschaften 84, 421-423. (doi:10.1007/s001140050422)
53. Meÿer, C. G., Holland, K. N. & Papastamatiou, Y. P. 2005 Sharks can detect changes in the geomagnetic field. J. R. Soc. Interface 2, 129-130. (doi:10.1098/rsif.2004.0021)
54. Molteno, T. C. A. & Kennedy, W. L. 2009 Navigation by induction-based magnetoreception in elasmobranch fishes. J. Biophys. 2009, 380976. (doi:10.1155/2009/380976)
55. Mora, C. V., Davison, M., Wild, J. M. & Walker, M. M. 2004 Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432, 508-511. (doi:10.1038/nature03077)
56. Mora, C. V., Davison, M. & Walker, M. M. 2009 Conditioning as a technique for studying the sensory systems involved in animal orientation, homing and navigation. J. Navig. 62, 571-585. (doi:10.1017/S0373463309990063)
57. Mouritsen, H., Feenders, G., Liedvogel, M. & Kropp, W. 2004a Migratory birds use head scans to detect the direction of the Earth's magnetic field. Curr. Biol. 14, 1946-1949. (doi:10.1016/j.cub.2004.10.025)
58. Mouritsen, H., Janssen-Bienhold, U., Liedvogel, M., Feenders, G., Stalleicken, J., Dirks, P. & Weiler, R. 2004b Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proc. Natl Acad. Sci. USA 101, 14 294-14 299. (doi:10.1073/pnas.0405968101)
59. Phillips, J. B. 1986 Two magnetoreception pathways in a migratory salamander. Science 233, 765-767. (doi:10.1126/science.3738508)
60. Reille, A. 1968 Essai de mise en evidence d'une sensibilite du pigeon au champ magnetique i l'aide d'un conditionnement nociceptif. J. Physiol. (Paris) 60, 85-92.
61. Ritz, T., Adem, S. & Schulten, K. 2000 A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707-718. (doi:10.1016/S0006-3495(00)76629-X)
62. Ritz, T., Thalau, P., Phillips, J. B., Wiltschko, R. & Wiltschko, W. 2004 Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429, 177-180. (doi:10.1038/nature02534)
63. Ritz, T., Wiltschko, R., Hore, P. J., Rodgers, C. T., Stapput, K., Thalau, P., Timmel, C. R. & Wiltschko, W. 2009 Magnetic compass of birds is based on a molecule with optimal directional sensitivity. Biophys. J. 96, 3451-3457. (doi:10.1016/j.bpj.2008.11.072)
64. Rodgers, C. T. & Hore, P. J. 2009 Chemical magnetoreception in birds: the radical pair mechanism. Proc. Natl Acad. Sci. USA 106, 353-360. (doi:10.1073/pnas.0711968106)
65. Rodgers, C. T., Henbest, K. B., Kukura, P., Timmel, C. R. & Hore, P. J. 2005 Low-field optically detected EPR spectroscopy of transient photoinduced radical pairs. J. Phys. Chem. A 109, 5035-5041. (doi:10.1021/jp050765z)
66. Rosenblum, B., Jungerman, R. L. & Longfellow, L. 1985 Limits to induction-based magnetoreception. In Magnetite biomineralization and magnetoreception in organisms: a new biomagnetism (eds J. L. Kirschvink, D. S. Jones & B. J. MacFadden), pp. 223-232. New York, NY: Plenum Press.
67. Rutledge, D. B. 1999 The electronics of radio. Cambridge, UK: Cambridge University Press.
68. Sancar, A. 2000 Cryptochrome: the second photoactive pigment in the eye and its role in circadian photoreception. Annu. Rev. Biochem. 69, 31-67. (doi:10.1146/annurev.biochem.69.1.31)
69. Schulten, K. 1982 Magnetic field effects in chemisty and biology. In Festkörperprobleme (Advances in solid state physics), vol. XXII (ed. J. Treusch), pp. 61-83. Braunschweig, Germany: Vieweg.
70. Shcherbakov, D., Winklhofer, M., Petersen, N., Steidle, J., Hilbig, R. & Blum, M. 2005 Magnetosensation in zebrafish. Curr. Biol. 15, R161-R162. (doi:10.1016/j.cub.2005.02.039)
71. Stapput, K., Thalau, H. P., Wiltschko, R. & Wiltschko, W. 2008 Orientation of birds in total darkness. Curr. Biol. 18, 602-606. (doi:10.1016/j.cub.2008.03.046)
72. Thalau, P., Ritz, T., Stapput, K.,Wiltschko, R. &Wiltschko,W. 2005 Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften 92, 86-90. (doi:10.1007/s00114-004-0595- 8)
73. Thalau, P., Ritz, T., Burda, H.,Wegner, R. E. & Wiltschko, R. 2006 The magnetic compass mechanisms of birds and rodents are based on different physical principles. J. R. Soc Interface 3, 583-587. (doi:10.1098/rsif.2006. 0130)
74. Tian, L., Xiao, B., Lin, W., Zhang, S., Zhu, R. & Pan, Y. 2007 Testing for the presence of magnetite in the upper-beak skin of homing pigeons. Biometals 20, 197-203. (doi:10.1007/s10534-006-9027-x)
75. Tuvia, S., Almagor, A., Bitler, A., Levin, S., Korenstein, R. & Yedgar, S. 1997 Cell membrane fluctuations are regulated by medium macroviscosity: evidence for a metabolic driving force. Proc. Natl Acad. Sci. USA 94, 5045-5049. (doi:10.1073/pnas.94.10.5045)
76. Walcott, C., Gould, J. L. & Kirschvink, J. L. 1979 Pigeons have magnets. Science 205, 1027-1029. (doi:10.1126/science.472725)
77. Walker, M. M. 1984 Learned magnetic field discrimination in yellowfin tuna, Thunnus albacares. J. Comp. Phys. A. 155, 673-679. (doi:10.1007/ BF00610853)
78. Walker, M. M. & Bitterman, M. E. 1985 Conditioned responding to magnetic fields by honeybees. J. Comp. Phys. A 157, 67-73. (doi:10.1007/ BF00611096)
79. Walker, M. M. & Bitterman, M. E. 1989 Honeybees can be trained to respond to very small changes in geomagnetic field intensity. J. Exp. Biol. 145, 489-494.
80. Walker, M. M., Baird, D. L. & Bitterman, M. E. 1989 Failure of stationary but not of flying honeybees to respond to magnetic field stimulae. J. Comp. Psychol. 103, 62-69. (doi:10.1037/0735-7036.103.1.62)
81. Walker, M. M., Kirschvink, J. L., Dizon, A. E. & Ahmed, G. 1992 Evidence that fin whales respond to the geomagnetic field during migration. J. Exp. Biol. 171, 67-78.
82. Walker, M. M., Diebel, C. E., Haugh, C. V., Pankhurst, P. M., Montgomery, J. C. & Green, C. R. 1997 Structure and function of the vertebrate magnetic sense. Nature 390, 371-376. (doi:10.1038/37057)
83. Walker, M. M., Dennis, T. E. & Kirschvink, J. L. 2002 The magnetic sense and its use in long-distance navigation by animals. Curr. Opin. Neurobiol. 12, 735-744. (doi:10.1016/S0959-4388(02)00389-6)
84. Wiltschko, R. & Wiltschko, W. 1995 Magnetic orientation in animals. Zoophysiology, vol. 33. Berlin, Germany: Springer.
85. Wiltschko, R., Stapput, K., Ritz, T., Thalau, P. & Wiltschko, W. 2007 Magnetoreception in birds: different physical processes for two types of directional responses. HFSP J. 1, 41-48. (doi:10.2976/1.2714294)
86. Wiltschko, W., Munro, U., Wiltschko, R. & Kirschvink, J. L. 2002 Magnetite-based magnetoreception in birds: the effect of a biasing field and a pulse on migratory behavior. J. Exp. Biol. 205, 3031-3037.
87. Wiltschko, W., Ford, H., Munro, U., Winklhofer, M. & Wiltschko, R. 2007 Magnetite-based magnetoreception: the effect of repeated pulsing on the orientation of migratory birds. J. Comp. Physiol. A 193, 515-522. (doi:10.1007/s00359-006-0207-5)
88. Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. 2009 Avian orientation: the pulse effect is mediated by the magnetite receptors in the upper beak. Proc. R. Soc. B 276, 2227-2232. (doi:10.1098/rspb.2009.0050)
89. Winklhofer, M. 2009 The physics of geomagnetic-field transduction in animals. IEEE Trans. Magn. 42, 5259-5265. (doi:10.1109/TMAG.2009.2017940)
90. Winklhofer, M. & Kirschvink, J. L. 2010 A quantitative assessment of torque-transducer models for magnetoreception. J. R. Soc. Interface 7, S273-S289. (doi:10.1098/rsif.2009.0435.focus)
91. Winklhofer, M., Holtkamp-Rotzler, E., Hanzlik, M., Fleissner, G. & Petersen, N. 2001 Clusters of superparamagnetic magnetite particles in the upper-beak skin of homing pigeons: evidence of a magnetoreceptor? Eur. J. Minerol. 13, 659-669. (doi:10.1127/0935-1221/2001/0013-0659)
92. Yorke, E. D. 1979 A possible magnetic transducer in birds. J. Theor. Biol. 77, 101-105. (doi:10.1016/0022-5193(79)90140-1)
93. Zapka, M. et al. 2009 Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461, 1274-1277. (doi:10.1038/nature08528)
94. Zurkiya, O., Chan, A. W. S. & Hu, X. P. 2008 MagA is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter. Magn. Reson. Med. 59, 1225-1231. (doi:10.1002/mrm.21606)