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The rotating magnetocaloric effect as a potential mechanism for natural magnetic senses


Autoři: A. Martin Bell aff001;  Jacob T. Robinson aff002
Působiště autorů: Applied Physics Program, Rice University, Houston, Texas, United States of America aff001;  Department of Electrical and Computer Engineering, Rice University, Houston, Texas, United States of America aff002;  Department of Bioengineering, Rice University, Houston, Texas, United States of America aff003;  Department of Neuroscience, Baylor College of Medicine, Houston, Texas, United States of America aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222401

Souhrn

Many animals are able to sense the earth’s magnetic field, including varieties of arthropods and members of all major vertebrate groups. While the existence of this magnetic sense is widely accepted, the mechanism of action remains unknown. Building from recent work on synthetic magnetoreceptors, we propose a new model for natural magnetosensation based on the rotating magnetocaloric effect (RME), which predicts that heat generated by magnetic nanoparticles may allow animals to detect features of the earth’s magnetic field. Using this model, we identify the conditions for the RME to produce physiological signals in response to the earth’s magnetic field and suggest experiments to distinguish between candidate mechanisms of magnetoreception.

Klíčová slova:

Anisotropy – Entropy – Nanoparticles – Magnetic fields – Aspect ratio – Cell polarity – Magnetite


Zdroje

1. Johnsen S, Lohmann KJ. The physics and neurobiology of magnetoreception. Nature Reviews Neuroscience. 2005;6(9):703–712. doi: 10.1038/nrn1745 16100517

2. Hore PJ, Mouritsen H. The Radical-Pair Mechanism of Magnetoreception. Annual Review of Biophysics. 2016;45(1):299–344. doi: 10.1146/annurev-biophys-032116-094545 27216936

3. Lohmann KJ, Johnsen S. The neurobiology of magnetoreception in vertebrate animals. Trends in Neurosciences. 2000;23(4):153–159. doi: 10.1016/s0166-2236(99)01542-8 10717674

4. Nordmann GC, Hochstoeger T, Keays DA. Magnetoreception—A sense without a receptor. PLOS Biology. 2017;15(10):e2003234. doi: 10.1371/journal.pbio.2003234

5. Mouritsen H. Long-distance navigation and magnetoreception in migratory animals. Nature. 2018;558(7708):50–59. doi: 10.1038/s41586-018-0176-1 29875486

6. Holland RA, Kirschvink JL, Doak TG, Wikelski M. Bats use magnetite to detect the earth’s magnetic field. PLoS ONE. 2008;3(2):1–6. doi: 10.1371/journal.pone.0001676

7. Cain SD, Boles LC, Wang JH, Lohmann KJ. Magnetic Orientation and Navigation in Marine Turtles, Lobsters, and Molluscs: Concepts and Conundrums. Integrative and Comparative Biology. 2005;45(3):539–546. doi: 10.1093/icb/45.3.539 21676799

8. Kalmijn A. Biophysics of geomagnetic field detection. IEEE Transactions on Magnetics. 1981;17(1):1113–1124. doi: 10.1109/TMAG.1981.1061156

9. Rodgers CT, Hore PJ. Chemical magnetoreception in birds: the radical pair mechanism. Proceedings of the National Academy of Sciences of the United States of America. 2009;106(2):353–60. doi: 10.1073/pnas.0711968106 19129499

10. Kirschvink JL, Gould JL. Biogenic magnetite as a basis for magnetic field detection in animals. Bio Systems. 1981;13(3):181–201. doi: 10.1016/0303-2647(81)90060-5 7213948

11. Davila AF, Fleissner G, Winklhofer M, Petersen N. A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite. Physics and Chemistry of the Earth, Parts A/B/C. 2003;28(16-19):647–652. doi: 10.1016/S1474-7065(03)00118-9

12. Wiltschko W, Wiltschko R. Magnetic orientation and magnetoreception in birds and other animals. Journal of comparative physiology A, Neuroethology, sensory, neural, and behavioral physiology. 2005;191(8):675–93. doi: 10.1007/s00359-005-0627-7 15886990

13. Uebe R, Schüler D. Magnetosome biogenesis in magnetotactic bacteria. Nature Reviews Microbiology. 2016;14(10):621–637. doi: 10.1038/nrmicro.2016.99 27620945

14. Lohmann KJ, Lohmann CMF, Putman NF. Magnetic maps in animals: nature’s GPS. Journal of Experimental Biology. 2007;210(21):3697–3705. doi: 10.1242/jeb.001313

15. Shaw J, Boyd A, House M, Woodward R, Mathes F, Cowin G, et al. Magnetic particle-mediated magnetoreception. Journal of The Royal Society Interface. 2015;12(110):20150499. doi: 10.1098/rsif.2015.0499

16. Mouritsen H, Hore PJ. The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds. Current opinion in neurobiology. 2012;22(2):343–52. doi: 10.1016/j.conb.2012.01.005 22465538

17. Phillips JB, Jorge PE, Muheim R. Light-dependent magnetic compass orientation in amphibians and insects: candidate receptors and candidate molecular mechanisms. Journal of The Royal Society Interface. 2010;7(Suppl_2):S241–S256. doi: 10.1098/rsif.2009.0459.focus

18. Wheeler MA, Smith CJ, Ottolini M, Barker BS, Purohit AM, Grippo RM, et al. Genetically targeted magnetic control of the nervous system. Nature Neuroscience. 2016;19(5):756–761. doi: 10.1038/nn.4265 26950006

19. Duret G, Polali S, Anderson ED, Bell AM, Tzouanas CN, Avants BW, et al. Magnetic entropy as a proposed gating mechanism for magnetogenetic ion channels. Biophysical Journal. 2019; p. 148379.

20. Piñol R, Brites CDS, Bustamante R, Martínez A, Silva NJO, Murillo JL, et al. Joining time-resolved thermometry and magnetic-induced heating in a single nanoparticle unveils intriguing thermal properties. ACS Nano. 2015;9(3):3134–3142. doi: 10.1021/acsnano.5b00059 25693033

21. Polo-Corrales L, Rinaldi C. Monitoring iron oxide nanoparticle surface temperature in an alternating magnetic field using thermoresponsive fluorescent polymers. Journal of Applied Physics. 2012;111(7):07B334. doi: 10.1063/1.3680532

22. Riedinger A, Guardia P, Curcio A, Garcia MA, Cingolani R, Manna L, et al. Subnanometer Local Temperature Probing and Remotely Controlled Drug Release Based on Azo-Functionalized Iron Oxide Nanoparticles. Nano Letters. 2013;13(6):2399–2406. doi: 10.1021/nl400188q 23659603

23. Martínez L, Figueira ACM, Webb P, Polikarpov I, Skaf MS. Mapping the Intramolecular Vibrational Energy Flow in Proteins Reveals Functionally Important Residues. The Journal of Physical Chemistry Letters. 2011;2(16):2073–2078. doi: 10.1021/jz200830g

24. Balli M, Jandl S, Fournier P, Gospodinov MM. Anisotropy-enhanced giant reversible rotating magnetocaloric effect in HoMn 2 O 5 single crystals. Applied Physics Letters. 2014;104(23):232402. doi: 10.1063/1.4880818

25. Arakaki A, Yamagishi A, Fukuyo A, Tanaka M, Matsunaga T. Co-ordinated functions of Mms proteins define the surface structure of cubo-octahedral magnetite crystals in magnetotactic bacteria. Molecular Microbiology. 2014;93(3):554–567. doi: 10.1111/mmi.12683 24961165

26. Li J, Menguy N, Gatel C, Boureau V, Snoeck E, Patriarche G, et al. Crystal growth of bullet-shaped magnetite in magnetotactic bacteria of the Nitrospirae phylum. Journal of The Royal Society Interface. 2015;12(103):20141288–20141288. doi: 10.1098/rsif.2014.1288

27. Yamagishi A, Tanaka M, Lenders JJM, Thiesbrummel J, Sommerdijk NAJM, Matsunaga T, et al. Control of magnetite nanocrystal morphology in magnetotactic bacteria by regulation of mms7 gene expression. Scientific Reports. 2016;6(1):29785. doi: 10.1038/srep29785 27417732

28. Grohe B, O’Young J, Ionescu DA, Lajoie G, Rogers KA, Karttunen M, et al. Control of Calcium Oxalate Crystal Growth by Face-Specific Adsorption of an Osteopontin Phosphopeptide. Journal of the American Chemical Society. 2007;129(48):14946–14951. doi: 10.1021/ja0745613 17994739

29. Collins BA. A comparison of the size of photoreceptor cells from the retina of the domestic pig as determined by light and scanning electron microscopy. Micron and Microscopica Acta. 1986;17(3):259–267. doi: 10.1016/0739-6260(86)90007-9

30. Nadol JB. Synaptic morphology of inner and outer hair cells of the human organ of Corti. Journal of Electron Microscopy Technique. 1990;15(2):187–196. doi: 10.1002/jemt.1060150210 2355269

31. Schultens HA, Schild D. Biophysical Properties of Olfactory Receptor Neurones. In: Sensors and Sensory Systems for an Electronic Nose. Dordrecht: Springer Netherlands; 1992. p. 13–24. Available from: http://link.springer.com/10.1007/978-94-015-7985-8_2.

32. Ma H, Yang R, Thomas SM, Kinnamon JC. Qualitative and quantitative differences between taste buds of the rat and mouse. BMC neuroscience. 2007;8(1):5. doi: 10.1186/1471-2202-8-5 17207280

33. Melemedjian OK, Khoutorsky A. Translational Control of Chronic Pain. vol. 131. 1st ed. Elsevier Inc.; 2015. Available from: http://doi.org/10.1016/bs.pmbts.2014.11.006.

34. Vacher H, Mohapatra DP, Trimmer JS. Localization and Targeting of Voltage-Dependent Ion Channels in Mammalian Central Neurons. Physiological Reviews. 2008;88(4):1407–1447. doi: 10.1152/physrev.00002.2008 18923186

35. Lai HC, Jan LY. The distribution and targeting of neuronal voltage-gated ion channels. Nature Reviews Neuroscience. 2006;7(7):548–562. doi: 10.1038/nrn1938 16791144

36. Reeves DB, Weaver JB. Approaches for modeling magnetic nanoparticle dynamics. Critical reviews in biomedical engineering. 2014;42(1):85–93. doi: 10.1615/CritRevBiomedEng.2014010845 25271360

37. Ramesh A, Jiles DC, Bi Y. Generalization of hysteresis modeling to anisotropic materials. Journal of Applied Physics. 1997;81(8):5585–5587. doi: 10.1063/1.364843

38. Franco V, Blázquez J, Ingale B, Conde A. The Magnetocaloric Effect and Magnetic Refrigeration Near Room Temperature: Materials and Models. Annual Review of Materials Research. 2012;42(1):305–342. doi: 10.1146/annurev-matsci-062910-100356

39. Gorobets O, Gorobets S, Koralewski M. Physiological origin of biogenic magnetic nanoparticles in health and disease: from bacteria to humans. International Journal of Nanomedicine. 2017;Volume 12:4371–4395. doi: 10.2147/IJN.S130565

40. Winklhofer M. Magnetoreception. Journal of The Royal Society Interface. 2010;7(Suppl_2):S131–S134. doi: 10.1098/rsif.2010.0010.focus

41. Lohmann KJ. Magnetic Remanence In The Western Atlantic Spiny Lobster, Panulirus-Argus. Journal of Experimental Biology. 1984;113(NOV):29–41.

42. Kletetschka G, Wasilewski PJ. Grain size limit for SD hematite. Physics of the Earth and Planetary Interiors. 2002;129(1-2):173–179. doi: 10.1016/S0031-9201(01)00271-0

43. Stacey FD. The physical theory of rock magnetism. Advances in Physics. 1963;12(45):45–133. doi: 10.1080/00018736300101263

44. Minke B, Cook B. TRP Channel Proteins and Signal Transduction. Physiological Reviews. 2002;82(2):429–472. doi: 10.1152/physrev.00001.2002 11917094

45. Bruno P. Physical origins and theoretical models of magnetic anisotropy. In: Physical origins and theoretical models of magnetic anisotropy. vol. 65; 1993. p. 257.

46. Martínez-Pérez MJ, de Miguel R, Carbonera C, Martínez-Júlvez M, Lostao A, Piquer C, et al. Size-dependent properties of magnetoferritin. Nanotechnology. 2010;21(46):465707. doi: 10.1088/0957-4484/21/46/465707 20975213

47. Řezníček R, Chlan V, Štěpánková H, Novák P, Maryško M. Magnetocrystalline anisotropy of magnetite. Journal of Physics: Condensed Matter. 2012;24(5):055501. doi: 10.1088/0953-8984/24/5/055501 22227433

48. Chiolerio A, Chiodoni A, Allia P, Martino P. Magnetite and Other Fe-Oxide Nanoparticles. In: Handbook of Nanomaterials Properties. Berlin, Heidelberg: Springer Berlin Heidelberg; 2014. p. 213–246. Available from: http://materials.springer.com/bp/docs/978-3-642-31107-9http://materials.springer.com/lb/docs/sm_smf_978-3-642-31107-9_34.

49. Mercante LA, Melo WWM, Granada M, Troiani HE, MacEdo WAA, Ardison JD, et al. Magnetic properties of nanoscale crystalline maghemite obtained by a new synthetic route. Journal of Magnetism and Magnetic Materials. 2012;324(19):3029–3033. doi: 10.1016/j.jmmm.2012.04.049

50. Martin-Hernandez F, Guerrero-Suárez S. Magnetic anisotropy of hematite natural crystals: High field experiments. International Journal of Earth Sciences. 2012;101(3):637–647. doi: 10.1007/s00531-011-0665-z

51. Özdemir Ö, Dunlop DJ. Hysteresis and coercivity of hematite. Journal of Geophysical Research: Solid Earth. 2014;119(4):2582–2594.

52. Silva NJO, Amaral VS, Carlos LD, Rodríguez-González B, Liz-Marzán LM, Millan A, et al. Structural and magnetic studies in ferrihydrite nanoparticles formed within organic-inorganic hybrid matrices. Journal of Applied Physics. 2006;100(5):054301. doi: 10.1063/1.2336083

53. Wang X, Zhu M, Koopal LK, Li W, Xu W, Liu F, et al. Effects of crystallite size on the structure and magnetism of ferrihydrite. Environmental Science: Nano. 2016;3(1):190–202.

54. Schrön A, Rödl C, Bechstedt F. Crystalline and magnetic anisotropy of the 3d-transition metal monoxides MnO, FeO, CoO, and NiO. Physical Review B. 2012;86(11):115134. doi: 10.1103/PhysRevB.86.115134

55. Chen CJ, Chiang RK, Lai HY, Lin CR. Characterization of monodisperse wüstite nanoparticles following partial oxidation. Journal of Physical Chemistry C. 2010;114(10):4258–4263. doi: 10.1021/jp908153y

56. Roberts AP, Chang L, Rowan CJ, Horng CS, Florindo F. Magnetic properties of sedimentary greigite (Fe 3 S 4): An update. Reviews of Geophysics. 2011;49(1):RG1002. doi: 10.1029/2010RG000336

57. Martin-Hernandez F, García-Hernández MM. Magnetic properties and anisotropy constant of goethite single crystals at saturating high fields. Geophysical Journal International. 2010;181(2):756–761.

58. Jandacka P, Burda H, Pistora J. Magnetically induced behaviour of ferritin corpuscles in avian ears: can cuticulosomes function as magnetosomes? Journal of The Royal Society Interface. 2014;12(102):20141087–20141087.

59. de Oliveira JF, Wajnberg E, de Souza Esquivel DM, Weinkauf S, Winklhofer M, Hanzlik M. Ant antennae: are they sites for magnetoreception? Journal of The Royal Society Interface. 2010;7(42):143–152.

60. Yuan Z, Atanassov P, Alsmadi AM, te Velthuis SGE, Welp U, Hammetter CI, et al. Magnetic properties of self-assembled ferritin-core arrays. Journal of Applied Physics. 2006;99(8):08Q509. doi: 10.1063/1.2172546

61. Quintana C, Cowley JM, Marhic C. Electron nanodiffraction and high-resolution electron microscopy studies of the structure and composition of physiological and pathological ferritin. Journal of Structural Biology. 2004;147(2):166–178. doi: 10.1016/j.jsb.2004.03.001 15193645

62. Galvez N, Ceoli M, Clemente-Leo M, Lo M, Calvino JJ, Ste O, et al. Comparative Structural and Chemical Studies of Ferritin. Journal of the American Chemical Society. 2008;130(5):8062–8068. doi: 10.1021/ja800492z 18507465

63. Jiles DC, Atherton DL. Theory of the magnetisation process in ferromagnets and its application to the magnetomechanical effect. Journal of Physics D: Applied Physics. 1984;17(6):1265–1281. doi: 10.1088/0022-3727/17/6/023

64. Raghunathan A, Melikhov Y, Snyder JE, Jiles DC. Generalized form of anhysteretic magnetization function for Jiles–Atherton theory of hysteresis. Applied Physics Letters. 2009;95(17):172510. doi: 10.1063/1.3249581

65. Fannin PC, Charles SW. On the calculation of the Neel relaxation time in uniaxial single-domain ferromagnetic particles. Journal of Physics D: Applied Physics. 1994;27(2):185–188. doi: 10.1088/0022-3727/27/2/001

66. Edelman NB, Fritz T, Nimpf S, Pichler P, Lauwers M, Hickman RW, et al. No evidence for intracellular magnetite in putative vertebrate magnetoreceptors identified by magnetic screening. Proceedings of the National Academy of Sciences. 2015;112(1):262–267. doi: 10.1073/pnas.1407915112

67. Treiber CD, Salzer MC, Riegler J, Edelman N, Sugar C, Breuss M, et al. Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature. 2012;484(7394):367–70. doi: 10.1038/nature11046 22495303

68. Patapoutian A, Peier AM, Story GM, Viswanath V. Sensory systems: ThermoTRP channels and beyond: mechanisms of temperature sensation. Nature Reviews Neuroscience. 2003;4(7):529–539. doi: 10.1038/nrn1141

69. Pertusa M, Moldenhauer H, Brauchi S, Latorre R, Madrid R, Orio P. Mutagenesis and Temperature-Sensitive Little Machines. In: Mutagenesis. InTech; 2012. p. 221–246. Available from: http://www.intechopen.com/books/mutagenesis/mutagenesis-and-temperature-sensitive-little-machines.

70. Noel J, Zimmermann K, Busserolles JJ, Deval E, Alloui A, Diochot S, et al. The mechano-activated K+ channels TRAAK and TREK-1 control both warm and cold perception. The EMBO journal. 2009;28(9):1308–1318. doi: 10.1038/emboj.2009.57 19279663

71. Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature. 2004;430(7001):748–754. doi: 10.1038/nature02732 15306801

72. Xu H, Ramsey IS, Kotecha SA, Moran MM, Chong JA, Lawson D, et al. TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature. 2002;418(6894):181–186. doi: 10.1038/nature00882 12077604

73. Güler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M. Heat-Evoked Activation of the Ion Channel, TRPV4. The Journal of Neuroscience. 2002;22(15):6408–6414.

74. Held K, Voets T, Vriens J. TRPM3 in temperature sensing and beyond. Temperature. 2015;2(3):201–213. doi: 10.4161/23328940.2014.988524

75. Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N, Ninomiya Y, et al. Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature. 2005;438(7070):1022–5. doi: 10.1038/nature04248 16355226

76. Brauchi S, Orio P, Latorre R. Clues to understanding cold sensation: Thermodynamics and electrophysiological analysis of the cold receptor TRPM8. Proceedings of the National Academy of Sciences. 2004;101(43):15494–15499. doi: 10.1073/pnas.0406773101

77. Zimmermann K, Lennerz JK, Hein A, Link AS, Kaczmarek JS, Delling M, et al. Transient receptor potential cation channel, subfamily C, member 5 (TRPC5) is a cold-transducer in the peripheral nervous system. Proceedings of the National Academy of Sciences. 2011;108(44):18114–18119. doi: 10.1073/pnas.1115387108

78. Ritz T, Adem S, Schulten K. A model for photoreceptor-based magnetoreception in birds. Biophysical Journal. 2000;78(2):707–718. doi: 10.1016/S0006-3495(00)76629-X 10653784

79. Heyers D, Manns M, Luksch H, Güntürkün O, Mouritsen H. A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLoS ONE. 2007;2(9). doi: 10.1371/journal.pone.0000937 17895978

80. Ra Holland, Helm B. A strong magnetic pulse affects the precision of departure direction of naturally migrating adult but not juvenile birds. Journal of The Royal Society Interface. 2013;10(81):20121047–20121047. doi: 10.1098/rsif.2012.1047

81. Wiltschko W, Munro U, Wiltschko R, Kirschvink JL. Magnetite-based magnetoreception in birds: the effect of a biasing field and a pulse on migratory behavior. J Exp Biol. 2002;205(Pt 19):3031–7. 12200406

82. Davila AF, Winklhofer M, Shcherbakov VP, Petersen N. Magnetic Pulse Affects a Putative Magnetoreceptor Mechanism. Biophysical Journal. 2005;89(1):56–63. doi: 10.1529/biophysj.104.049346 15863473

83. Holland RA. Differential effects of magnetic pulses on the orientation of naturally migrating birds. Journal of The Royal Society Interface. 2010;7(52):1617–1625. doi: 10.1098/rsif.2010.0159

84. Beason, Dussourd, Deutschlander. Behavioural evidence for the use of magnetic material in magnetoreception by a migratory bird. The Journal of experimental biology. 1995;198(Pt 1):141–6. 9317510

85. Wiltschko W, Wiltschko R. Migratory orientation of European Robins is affected by the wavelength of light as well as by a magnetic pulse. Journal of Comparative Physiology A. 1995;177(3):363–369. doi: 10.1007/BF00192425

86. Irwin WP, Lohmann KJ. Disruption of magnetic orientation in hatchling loggerhead sea turtles by pulsed magnetic fields. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology. 2005;191(5):475–480. doi: 10.1007/s00359-005-0609-9 15765235

87. Wiltschko W, Munro U, Beason RC, Ford H, Wiltschko R. A magnetic pulse leads to a temporary deflection in the orientation of migratory birds. Experientia. 1994;50(7):697–700. doi: 10.1007/BF01952877

88. Munro U, Munro JA, Phillips JB, Wiltschko W. Effect of wavelength of light and pulse magnetisation on different magnetoreception systems in a migratory bird. Australian Journal of Zoology. 1997;45(2):189–198. doi: 10.1071/ZO96066

89. Thébault E, Finlay CC, Beggan CD, Alken P, Aubert J, Barrois O, et al. International Geomagnetic Reference Field: the 12th generation. Earth, Planets and Space. 2015;67(1):79. doi: 10.1186/s40623-015-0228-9

90. Sanz-Salvador L, Andrés-Borderia A, Ferrer-Montiel A, Planells-Cases R. Agonist- and Ca2+-dependent desensitization of TRPV1 channel targets the receptor to lysosomes for degradation. Journal of Biological Chemistry. 2012;287(23):19462–19471. doi: 10.1074/jbc.M111.289751 22493457

91. Fatemi-Ardekani A. Transcranial magnetic stimulation: physics, electrophysiology, and applications.. vol. 36; 2008.

92. Ritz T, Thalau P, Phillips JB, Wiltschko R, Wiltschko W. Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature. 2004;429(6988):177–180. doi: 10.1038/nature02534 15141211

93. Maeda K, Henbest KB, Cintolesi F, Kuprov I, Rodgers CT, Liddell PA, et al. Chemical compass model of avian magnetoreception. Nature. 2008;453(7193):387–390. doi: 10.1038/nature06834 18449197

94. Deatsch AE, Evans BA. Heating efficiency in magnetic nanoparticle hyperthermia. Journal of Magnetism and Magnetic Materials. 2014;354:163–172. doi: 10.1016/j.jmmm.2013.11.006

95. Rosensweig RE. Heating magnetic fluid with alternating magnetic field. Journal of Magnetism and Magnetic Materials. 2002;252(1-3 SPEC. ISS.):370–374. doi: 10.1016/S0304-8853(02)00706-0

96. Keary N, Ruploh T, Voss J, Thalau P, Wiltschko R, Wiltschko W, et al. Oscillating magnetic field disrupts magnetic orientation in Zebra finches, Taeniopygia guttata. Frontiers in zoology. 2009;6:25. doi: 10.1186/1742-9994-6-25

97. Schwarze S, Schneider NL, Reichl T, Dreyer D, Lefeldt N, Engels S, et al. Weak Broadband Electromagnetic Fields are More Disruptive to Magnetic Compass Orientation in a Night-Migratory Songbird (Erithacus rubecula) than Strong Narrow-Band Fields. Frontiers in Behavioral Neuroscience. 2016;10(March):1–13.

98. Ritz T, Wiltschko R, Hore PJ, Rodgers CT, Stapput K, Thalau P, et al. Magnetic Compass of Birds Is Based on a Molecule with Optimal Directional Sensitivity. Biophysical Journal. 2009;96(8):3451–3457. doi: 10.1016/j.bpj.2008.11.072 19383488

99. Quinn TP, Merrill RT, Brannon EL. Magnetic field detection in sockeye salmon. Journal of Experimental Zoology. 1981;217(1):137–142. doi: 10.1002/jez.1402170114

100. Lohmann KJ, Pentcheff ND, Nevitt GA, Stetten GD, Zimmer-faust RK, Jarrard HE, et al. Magnetic orientation of spiny lobsters in the ocean: experiments with undersea coil systems. The Journal of experimental biology. 1995;198(Pt 10):2041–2048. 9319949

101. Marhold S, Wiltschko W, Burda H. A Magnetic Polarity Compass for Direction Finding in a Subterranean Mammal. Naturwissenschaften. 1997;84(9):421–423. doi: 10.1007/s001140050422

102. Muheim R, Bäckman J, Åkesson S. Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light. J Exp Biol. 2002;205:3845–3856. 12432008

103. Wiltschko W, Wiltschko R. Light-dependent magnetoreception in birds: the behaviour of European robins, Erithacus rubecula, under monochromatic light of various wavelengths and intensities. The Journal of experimental biology. 2001;204:3295–3302. 11606603

104. Pinzon-Rodriguez A, Muheim R. Zebra finches have a light-dependent magnetic compass similar to migratory birds. The Journal of Experimental Biology. 2017;220(7):1202–1209. doi: 10.1242/jeb.148098 28356366

105. Phillips JB, Borland SC. Behavioural evidence for use of a light-dependent magnetoreception mechanism by a vertebrate. Nature. 1992;359(6391):142–144. doi: 10.1038/359142a0

106. Timmel CR, Hore PJ. Oscillating magnetic field effects on the yields of radical pair reactions. Chemical Physics Letters. 1996;257(3-4):401–408. doi: 10.1016/0009-2614(96)00466-6


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