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A Model for Photoreceptor-Based Magnetoreception in Birds
Open accessAbstract
A large variety of animals has the ability to sense the geomagnetic field and utilize it as a source of directional (compass) information. It is not known by which biophysical mechanism this magnetoreception is achieved. We investigate the possibility that magnetoreception involves radical-pair processes that are governed by anisotropic hyperfine coupling between (unpaired) electron and nuclear spins. We will show theoretically that fields of geomagnetic field strength and weaker can produce significantly different reaction yields for different alignments of the radical pairs with the magnetic field. As a model for a magnetic sensory organ we propose a system of radical pairs being 1) orientationally ordered in a molecular substrate and 2) exhibiting changes in the reaction yields that affect the visual transduction pathway. We evaluate three-dimensional visual modulation patterns that can arise from the influence of the geomagnetic field on radical-pair systems. The variations of these patterns with orientation and field strength can furnish the magnetic compass ability of birds with the same characteristics as observed in behavioral experiments. We propose that the recently discovered photoreceptor cryptochrome is part of the magnetoreception system and suggest further studies to prove or disprove this hypothesis.
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“In recent years, quantum biology too has been benefitting considerably from the refinement of experimental tools that are beginning to provide direct access to the observation of quantum dynamics in biological systems [11-14]”
From Vibrations, quanta and biology (2013) · cites this paper as [11]
In the citing paper
“environment assisted excitation energy transport in photosynthesis [11, 15, 16], magneto-reception of birds [17-19] and the mechanism underlying olfaction [20, 21], for which there is some compelling theoretical and/or experimental evidence that quantum phenomena are essential for their understanding.”
From Vibrations, quanta and biology (2013) · cites this paper as [11]
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“At the same time, it has been shown in experimental models that in “warm and wet” birds, quantum entanglement and coherence may be involved in magnetic direction finding (Ritz et al., 2000).”
BackgroundRemoval of the local geomagnetic field affects reproductive growth in Arabidopsis
Xu, C., Wei, S., Lü, Y., Zhang, Y., Chen, C., & Song, T. (2013) · Bioelectromagnetics · doi:10.1002/bem.21788 · Cited by 44
“The blue light receptor, cryptochrome, was demonstrated to be involved in magnetoreception from the study of migratory birds, Drosophila, and Arabidopsis [Ritz et al., 2000, 2004; Mouristen et al., 2004; Ahmad et al., 2007; Liedvogel et al., 2007; Gegear et al., 2008].”
Backgroundvan Schooten, K. J., Baird, D., Limes, M. E., Lupton, J. M., & Boehme, C. (2015) · Nature Communications · doi:10.1038/ncomms7688 · Cited by 40
An improved semiclassical theory of radical pair recombination reactions
Manolopoulos, D. E., & Hore, P. J. (2013) · The Journal of Chemical Physics · doi:10.1063/1.4821817 · Cited by 44
Gibberellins are involved in effect of near‐null magnetic field on Arabidopsis flowering
Xu, C., Yu, Y., Zhang, Y., Li, Y., & Wei, S. (2016) · Bioelectromagnetics · doi:10.1002/bem.22004 · Cited by 43
“To disclose the mechanism of magnetoreception, cryptochrome was suggested to be a magnetoreceptor based on radical-pair mechanism and research on the magnetic field response of Drosophila cry mutants [Ritz et al., 2000; Gegear et al., 2008, 2010; Foley et al., 2011; Maeda et al., 2012].”
BackgroundMyklatun, A., Lauri, A., Eder, S. H. K., Cappetta, M., Shcherbakov, D., Wurst, W., Michael Winklhofer, A., & Westmeyer, G. G. (2018) · Nature Communications · doi:10.1038/s41467-018-03090-6 · Cited by 44
The brain of a nocturnal migratory insect, the Australian Bogong moth
Adden, A. K., Wibrand, S., Pfeiffer, K., Warrant, E. J., & Heinze, S. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.24866 · Cited by 44
“hypothesis across many animal species (Ritz et al. 2000; Schulten et al. 1978), including in”
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Cai, C. Y., Ai, Q., Quan, H. T., & Sun, C. P. (2012) · Physical Review A · doi:10.1103/physreva.85.022315 · Cited by 42
Schwarze, S., Steenken, F., Thiele, N., Kobylkov, D., Lefeldt, N., Dreyer, D., Schneider, N.-L., & Mouritsen, H. (2016) · Scientific Reports · doi:10.1038/srep33805 · Cited by 43
Very weak oscillating magnetic field disrupts the magnetic compass of songbird migrants
Pakhomov, A. Y., Bojarinova, J., Cherbunin, R. V., Chetverikova, R., Grigoryev, P. S., Kavokin, K. V., Kobylkov, D., Lubkovskaja, R., & Chernetsov, N. (2017) · Journal of The Royal Society Interface · doi:10.1098/rsif.2017.0364 · Cited by 43
Upper bound on the biological effects of 50/60 Hz magnetic fields mediated by radical pairs
Hore, P. J. (2019) · eLife · doi:10.7554/elife.44179 · Cited by 43
“It now seems likely that migratory songbirds detect the 50 direction of the geomagnetic field by means of photo-induced radical pairs generated within 51 cryptochrome proteins located in their retinas (24, 28, 29).”
BackgroundMagnetoreception and magnetic navigation in fishes: a half century of discovery
Naisbett‐Jones, L. C., & Lohmann, K. J. (2022) · Journal of Comparative Physiology A · doi:10.1007/s00359-021-01527-w · Cited by 50
Chetverikova, R., Dautaj, G., Schwigon, L., Dedek, K., & Mouritsen, H. (2022) · Journal of The Royal Society Interface · doi:10.1098/rsif.2021.0877 · Cited by 42
(2014) · Advances in the study of behavior · doi:10.1016/b978-0-12-800286-5.00002-x · Cited by 42
Binhi, V. N. (2008) · International Journal of Radiation Biology · doi:10.1080/09553000802195323 · Cited by 42
“Unlike studies of orientationally ordered RP in a mechanism of animal navigation (Ritz et al. 2000), it is not necessary here to take into account the particle orientation.”
BackgroundQuantum Probe and Design for a Chemical Compass with Magnetic Nanostructures
Cai, J. (2011) · Physical Review Letters · doi:10.1103/physrevlett.106.100501 · Cited by 41
Decoherence in the chemical compass: the role of decoherence for avian magnetoreception
Tiersch, M., & Briegel, H. J. (2012) · Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rsta.2011.0488 · Cited by 42
Oliveriusová, L., Němec, P., Králová, Z., & Sedláček, F. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.069625 · Cited by 41
“The light-induced radical pair mechanism appears to be intimately coupled with photoreception (Ritz et al., 2000; Rodgers and Hore, 2009) but not necessarily with image-forming vision.”
BackgroundMagnetic field effects in proteins
Jones, A. R. (2016) · Molecular Physics · doi:10.1080/00268976.2016.1149631 · Cited by 42
Low-Field Optically Detected EPR Spectroscopy of Transient Photoinduced Radical Pairs
Rodgers, C. T., Henbest, K. B., Kukura, P., Timmel, C. R., & Hore, P. J. (2005) · The Journal of Physical Chemistry A · doi:10.1021/jp050765z · Cited by 42
Bulte, M., Heyers, D., Mouritsen, H., & Bairlein, F. (2017) · Journal of Avian Biology · doi:10.1111/jav.01285 · Cited by 42
Geomagnetic field affects spring migratory direction in a long distance migrant
Henshaw, I., Fransson, T., Jakobsson, S., & Kullberg, C. (2010) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-010-0946-8 · Cited by 41
“As magnetic compass orientation in birds is believed to be light dependant (Ritz et al. 2000), a lightemitting diode (LED), 525 nm (green), gave an ambient light source not directly visible to the birds during the night (∼0.”
BackgroundInfluentialКрылов, В. В., Зотов, О. Д., Klain, B. I., Ушакова, Н. В., Канцерова, Н. П., Znobisheva, A. V., Izyumov, Y. G., Кузьмина, В. В., Morozov, A. A., Лысенко, Л. А., et al. (2014) · Journal of Atmospheric and Solar-Terrestrial Physics · doi:10.1016/j.jastp.2014.01.020 · Cited by 41
Immeln, D., Pokorny, R., Herman, E., Moldt, J., Batschauer, A., & Kottke, T. (2010) · The Journal of Physical Chemistry B · doi:10.1021/jp1076388 · Cited by 41
Coherent and incoherent theories for photosynthetic energy transfer
Tao, M.-J., Zhang, N.-N., Wen, P.-Y., Deng, F.-G., Ai, Q., & Long, G.-L. (2019) · 中国科学通报：英文版 · doi:10.1016/j.scib.2019.12.009 · Cited by 42
Wiltschko, R., Stapput, K., Bischof, H., & Wiltschko, W. (2007) · Frontiers in Zoology · doi:10.1186/1742-9994-4-5 · Cited by 41
Freake, M. J., & Phillips, J. B. (2005) · Ethology · doi:10.1111/j.1439-0310.2004.01067.x · Cited by 41
“…magnetic compass is light-dependent (Phillips & Borland 1992a, b; Deutschlander et al. 1999a; Phillips et al. 2001), and exhibits properties consistent with a photoreceptor-based magnetoreception mechanism involving a photoexcited radical pair reaction (Schulten & Windemuth 1986; Ritz et al. 2000).”
BackgroundMitsui, H., Maeda, T., Chiaki, Y., Tsuji, Y., Watari, R., Kubo, Y., Okano, K., & Okano, T. (2015) · Biochemistry · doi:10.1021/bi501441u · Cited by 40
Mani, T., Niedzwiedzki, D. M., & Vinogradov, S. A. (2012) · The Journal of Physical Chemistry A · doi:10.1021/jp301345h · Cited by 40
Miura, T., Maeda, K., & Arai, T. (2006) · The Journal of Physical Chemistry A · doi:10.1021/jp056488d · Cited by 40
Eumetazoan Cryptochrome Phylogeny and Evolution
Haug, M. F., Gesemann, M., Lazović, V., & Neuhauss, S. C. F. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv010 · Cited by 41
“The proposed molecule involved in the radical pair mechanism—one of the hypothesized mechanisms how the earth’s magnetic field could be detected (Ritz et al. 2000; Rodgers and Hore 2009)—is Cryptochrome (reviewed in Liedvogel and Mouritsen [2010]).”
BackgroundLefeldt, N., Dreyer, D., Steenken, F., Schneider, N.-L., & Mouritsen, H. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.107235 · Cited by 40
“Th e Jo ur na l o f E xp er im en ta l B io lo gy This is impressive, as it means that their magnetic compass sensory system (Ritz et al., 2000; Mouritsen et al., 2005; Heyers et al., 2007; Zapka et al., 2009; Rodgers and Hore, 2009; Treiber et al., 2012; Mouritsen and Hore, 2012) must be able to…”
BackgroundInfluentialAvian magnetic compass can be tuned to anomalously low magnetic intensities
Michael Winklhofer, A., Dylda, E., Thalau, P., Wiltschko, W., & Wiltschko, R. (2013) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.0853 · Cited by 40
“A radical pair process, which forms the physical basis of the avian inclination compass [8,9], was theoretically predicted to be effective in present-day Earthstrength fields, but whether it could cope with fields below 5 mT is unclear [10].”
BackgroundWiltschko, W., Möller, A., Gesson, M., Noll, C., & Wiltschko, R. (2004) · Journal of Experimental Biology · doi:10.1242/jeb.00873 · Cited by 40
“The radical pair model proposed by Schulten and Windemuth (1986) and Ritz et al. (2000) assumes that the direction of the geomagnetic field is perceived in the eye with the help of specialised photopigments.”
BackgroundMethodInfluentialThe radical pair mechanism and the avian chemical compass: Quantum coherence and entanglement
Zhang, Y., Berman, G. P., & Kais, S. (2015) · International Journal of Quantum Chemistry · doi:10.1002/qua.24943 · Cited by 41
“[41], we include only the Zeeman interaction and the hyperfine interaction in the Hamiltonian of the system:”
BackgroundMethodInfluentialO’Connell, C. P., Abel, D. C., Rice, P. H., Stroud, E. M., & Simuro, N. C. (2010) · Marine and Freshwater Behaviour and Physiology · doi:10.1080/10236241003672230 · Cited by 39
“…may perceive the Earth’s magnetic field through: (1) magnetite-based magnetoreception (Kirschvink et al. 2001; Wiltschko et al. 2002), (2) chemical magnetoreception (Ritz et al. 2000), or (3) indirect magnetoreception via electromagnetic induction (Kalmijn 1982, 1984; Johnsen and Lohmann 2005).”
BackgroundA New Type of Radical-Pair-Based Model for Magnetoreception
Stoneham, A. M., Gauger, E. M., Porfyrakis, K., Benjamin, S. C., & Lovett, B. W. (2012) · Biophysical Journal · doi:10.1016/j.bpj.2012.01.007 · Cited by 39
Mendive‐Tapia, D., Mangaud, É., Firmino, T. D. R., de la Lande, A., Desouter-Lecomte, M., Meyer, H., & Gatti, F. (2017) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.7b10412 · Cited by 40
Chernetsov, N. (2017) · Journal of Comparative Physiology A · doi:10.1007/s00359-016-1140-x · Cited by 39
“1978) and gained popularity when cryptochromes were proposed as possible magnetosensory molecules (Ritz et al. 2000), as they are the only known molecules in vertebrates that form radicals after photon absorption.”
BackgroundInfluentialNeurobiology of the homing pigeon—a review
Mehlhorn, J., & Rehkämper, G. (2009) · Die Naturwissenschaften · doi:10.1007/s00114-009-0560-7 · Cited by 40
“The triplet yield depends on the alignment of the molecules in the ambient magnetic field, which is position dependent and can thus convey information on magnetic directions (for details, see Ritz et al. 2000).”
BackgroundDirect Interaction of Avian Cryptochrome 4 with a Cone Specific G-Protein
Görtemaker, K., Yee, C., Bartölke, R., Behrmann, H., Voß, J.-O., Schmidt, J., Xu, J., Solovyeva, V., Leberecht, B., Behrmann, E., et al. (2022) · Cells · doi:10.3390/cells11132043 · Cited by 38
“(1978) proposed a radical-pair mechanism as the underlying mechanism for magnetic sensing [9], and a ubiquitously present class of chromophore proteins called cryptochromes (Cry) seemed to match the required properties for a magnetosensor [6,10,11].”
BackgroundDellis, A. T., & Kominis, I. K. (2011) · Biosystems · doi:10.1016/j.biosystems.2011.11.007 · Cited by 38
“…radical-ion pairs are understood to underlie the biochemical magnetic compass used by avian species to navigate in earth’s magnetic field (Ritz et al., 2000; Wiltschko and Wiltschko, 2005), as corroborated by several recent experiments (Ritz et al., 2004, 2009; Maeda et al., 2008; Zapka…”
BackgroundTreiber, C. D., Salzer, M. C., Breuss, M. W., Ushakova, L., Lauwers, M., Edelman, N. B., & Keays, D. A. (2013) · Communicative & Integrative Biology · doi:10.4161/cib.24859 · Cited by 38
“The first, a light dependent mechanism argues that the spin state of free radicals is influenced by the local magnetic environment which affects the reactivity of photosensitive molecules, that in turn alters neuronal activity.(1,2) The second hypothesis argues that magnetic information is transduced into neuronal imp…”
BackgroundCan disordered radical pair systems provide a basis for a magnetic compass in animals?
Hill, E. M., & Ritz, T. (2009) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0378.focus · Cited by 38
“The light receptor cryptochrome has been suggested as a potential photo-magnetoreceptor candidate (Ritz et al. 2000) with some recent studies supporting a role of cryptochromes in magnetoreception (Ahmad et al.”
BackgroundMethodInfluentialSelf-citationFunctional MRI and functional connectivity of the visual system of awake pigeons
Groof, G. D., Jonckers, E., Güntürkün, O., Denolf, P., Audekerke, J. V., & der Linden, A. V. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.10.044 · Cited by 38
“This unusual functional mode arises from the underlying physical processes: the avian magnetic compass is based on a radical pair mechanism [46] in the eye, where Cryptochrome 1a, the most likely candidate receptor molecule for mediating directional information, is located along the disks of the outer segments of the…”
BackgroundQuantum correlations at infinite temperature: The dynamical Nagaoka effect
Kanász-Nagy, M., Lovas, I., Grusdt, F., Greif, D., Greiner, M., & Demler, E. (2017) · Physical review. B./Physical review. B · doi:10.1103/physrevb.96.014303 · Cited by 37
Comparative properties and functions of type 2 and type 4 pigeon cryptochromes
Wang, X., Jing, C., Selby, C. P., Chiou, Y., Yang, Y., Wu, W., Sancar, A., & Wang, J. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2920-y · Cited by 38
One Actor, Multiple Roles: The Performances of Cryptochrome in Drosophila
Damulewicz, M., & Mazzotta, G. M. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00099 · Cited by 37
Rishabh, R., Zadeh‐Haghighi, H., Salahub, D. R., & Simon, C. (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1010198 · Cited by 38
“This model relies on the coherent spin dynamics of pairs of radicals involving the cryptochrome (CRY) protein [32].”
BackgroundWiltschko, R., & Wiltschko, W. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-1704-0_8 · Cited by 39
Крылов, В. В., & Osipova, E. A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241310989 · Cited by 40
“The inclination and/or intensity of an external magnetic field should affect the electron spin state of such radical pairs [56], i.”
BackgroundMagnetoreception systems in birds: A review of current research
Kishkinev, D., & Chernetsov, N. (2015) · Biology Bulletin Reviews · doi:10.1134/s2079086415010041 · Cited by 36
Babcock, N. S., & Kattnig, D. R. (2021) · JACS Au · doi:10.1021/jacsau.1c00332 · Cited by 37
Magnetic fields and fish behavior
Крылов, В. В., Izyumov, Y. G., Izvekov, E. I., & Nepomnyashchikh, V. A. (2014) · Biology Bulletin Reviews · doi:10.1134/s2079086414030049 · Cited by 37
“It is suggested that magnetoreception can be based on chemical reactions sensitive to the effect of the magnetic field (Philips and Borland, 1992; Ritz et al., 2000; Rodgers and Hore, 2009).”
Okano, H., Masuda, H., & Ohkubo, C. (2005) · Bioelectromagnetics · doi:10.1002/bem.20055 · Cited by 37
Wiltschko, W., Munro, U. H., FORD, H. A., & Wiltschko, R. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2003.2476 · Cited by 37
Directional compass preference for landing in water birds
Hart, V., Malkemper, E. P., Kušta, T., Begall, S., Nováková, P., Hanzal, V., Pleskač, L., Ježek, M., Policht, R., Husinec, V., et al. (2013) · Frontiers in Zoology · doi:10.1186/1742-9994-10-38 · Cited by 36
“Further, not necessarily alternative, yet in any case a speculative explanation is that retinal magnetoreception (sensu [17]) serves as an inclinometer to estimate and control the angle of descents.”
BackgroundMagnetoreception in birds: II. Behavioural experiments concerning the cryptochrome cycle
Wiltschko, R., Gehring, D., Denzau, S., Nießner, C., & Wiltschko, W. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.110981 · Cited by 36
“Th e Jo ur na l o f E xp er im en ta l B io lo gy KEY WORDS: Cryptochrome 1a, Flavin cycle, Photoreduction, Activated Cry1a, Radical pair mechanism, Migratory orientation”
Spin-selective recombination kinetics of a model chemical magnetoreceptor
Maeda, K., Wedge, C. J., Storey, J. G., Henbest, K. B., Liddell, P. A., Kodis, G., Gust, D., Hore, P. J., & Timmel, C. R. (2011) · Chemical Communications · doi:10.1039/c1cc11625h · Cited by 36
Effect of magnetic pulses on Caribbean spiny lobsters: implications for magnetoreception
Ernst, D. A., & Lohmann, K. J. (2016) · Journal of Experimental Biology · doi:10.1242/jeb.136036 · Cited by 36
“Most recent research has focused on two possible biophysical mechanisms: (1) chemically mediated magnetoreception (Ritz et al., 2000; Maeda et al., 2008; Liedvogel and Mouritsen, 2010); and (2) magnetite-based magnetoreception (Kirschvink et al.”
BackgroundAnimal Navigation: The Evolution of Magnetic Orientation
Gould, J. L. (2008) · Current Biology · doi:10.1016/j.cub.2008.03.052 · Cited by 36
Magnetic orientation in the mealworm beetle Tenebrio and the effect of light
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“Sensitivity to polarity is not consistent with a photoreceptor-based mechanism involving either magnetite (Edmonds, 1996) or a light-induced radical-pair reaction (Ritz et al., 2000).”
BackgroundWhy are living things sensitive to weak magnetic fields?
Liboff, A. R. (2013) · Electromagnetic Biology and Medicine · doi:10.3109/15368378.2013.809579 · Cited by 38
“Furthermore, cryptochrome lends itself to magnetochemical sensitivity because it forms radical pairs upon photoexcitation (Liedvogel and Mouritsen, 2010; Ritz et al., 2000).”
BackgroundBinhi, V. N. (2005) · Bioelectromagnetics · doi:10.1002/bem.20178 · Cited by 35
Suppression of Arabidopsis flowering by near‐null magnetic field is mediated by auxin
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Molecular dynamics simulations disclose early stages of the photo-activation of cryptochrome 4
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Biological Effects of Space Hypomagnetic Environment on Circadian Rhythm
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Biomedical Applications of Electromagnetic Detection: A Brief Review
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“The currently commonly recognized mechanism is the free radical pair mechanism [32].”
BackgroundBurda, H., Begall, S., Hart, V., Malkemper, E. P., Painter, M. S., & Phillips, J. B. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.24131-x · Cited by 35
Excited flavin and pterin coenzyme molecules in evolution
Kritsky, M. S., Telegina, T. A., Vechtomova, Y. L., Kolesnikov, M. P., Lyudnikova, T. A., & Голуб, О. А. (2010) · Biochemistry (Moscow) · doi:10.1134/s0006297910100020 · Cited by 35
Light-dependent magnetic compass in Iberian green frog tadpoles
Diego‐Rasilla, F. J., Luengo, R. M., & Phillips, J. B. (2010) · Die Naturwissenschaften · doi:10.1007/s00114-010-0730-7 · Cited by 34
“The light-dependent magnetic compass is proposed to involve a light-absorbing molecule that forms radical pair intermediates (radical pair mechanism; Schulten et al. 1978; Schulten 1982; Schulten and Windemuth 1986; Ritz et al. 2000; Cintolesi et al. 2003; Solov’yov et al. 2007; Rodgers and Hore 2009).”
BackgroundMaeda, K., Neil, S. R. T., Henbest, K. B., Weber, S., Schleicher, E., Hore, P. J., Mackenzie, S. R., & Timmel, C. R. (2011) · Journal of the American Chemical Society · doi:10.1021/ja206783t · Cited by 35
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Focus on quantum effects and noise in biomolecules
Fleming, G. R., Huelga, S. F., & Plenio, M. B. (2011) · New Journal of Physics · doi:10.1088/1367-2630/13/11/115002 · Cited by 37
“New Journal of Physics 13 (2011) 115002 1367-2630/11/115002+05$33.00 © IOP Publishing Ltd and Deutsche Physikalische Gesellschaft 2 compass (Ritz et al 2000 Biophys.”
BackgroundInfluentialAvian navigation and geographic positioning
Deutschlander, M. E., & Beason, R. C. (2014) · Journal of Field Ornithology · doi:10.1111/jofo.12055 · Cited by 34
The effect of radiofrequency radiation on DNA and lipid damage in female and male infant rabbits
Güler, G., Tomruk, A., Özgür, E., Şahin, D., Sepici, A., Altan, N., & Seyhan, N. (2011) · International Journal of Radiation Biology · doi:10.3109/09553002.2012.646349 · Cited by 34
“Th e other one is the so-called Radical Pair Mechanism (RPM) where low intensity magnetic fi elds can eff ectively increase the lifetime of free radicals (Brocklehurst and McLauchlan 1996, Chignell and Sik 1998, Ritz et al. 2000, 2004, 2010).”
BackgroundExperimental quantum simulation of Avian Compass in a nuclear magnetic resonance system
Pearson, J., Feng, G., Zheng, C., & Long, G. (2016) · Science China Physics Mechanics and Astronomy · doi:10.1007/s11433-016-0376-6 · Cited by 34
Genomic and Phenotypic Analyses Reveal Mechanisms Underlying Homing Ability in Pigeon
Shao, Y., Tian, H.-Y., Zhang, J., Kharrati-Koopaee, H., Guo, X., Zhuang, X.-L., Li, M., Nanaei, H. A., Tafti, E. D., Shojaei, B., et al. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz208 · Cited by 32
A novel isoform of cryptochrome 4 (Cry4b) is expressed in the retina of a night-migratory songbird
Einwich, A., Dedek, K., Seth, P. K., Laubinger, S., & Mouritsen, H. (2020) · Scientific Reports · doi:10.1038/s41598-020-72579-2 · Cited by 34
Müller, P., Brettel, K., Grama, L., Nyitrai, M., & Lukács, A. (2016) · ChemPhysChem · doi:10.1002/cphc.201501077 · Cited by 32
Magnet-induced disorientation in hatchling loggerhead sea turtles
Irwin, W. P., & Lohmann, K. J. (2003) · Journal of Experimental Biology · doi:10.1242/jeb.00108 · Cited by 34
“…might be tiny and dispersed throughout a large volume of tissue (Kirschvink et al., 2001), or the transduction process might occur as a set of chemical reactions, so that no obvious organ or structure devoted to magnetoreception necessarily exists (Deutschlander et al., 1999b; Ritz et al., 2000).”
BackgroundPainter, M. S., Dommer, D. H., Altizer, W. W., Muheim, R., & Phillips, J. B. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.077404 · Cited by 34
“…that form photo-excited radical pair intermediates sensitive to magnetic fields (radical pair mechanism or RPM) that in some animals may cause the magnetic field to be perceived as a pattern of light intensity superimposed on the animal’s surroundings (Ritz et al., 2000; Phillips et al., 2010b).”
InfluentialLinking magnetite in the abdomen of honey bees to a magnetoreceptive function
Lambinet, V., Hayden, M. E., Reigl, K., Gomis, S., & Gries, G. (2017) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2016.2873 · Cited by 33
The sacrificial inactivation of the blue-light photosensor cryptochrome from Drosophila melanogaster
Kutta, R. J., Archipowa, N., & Scrutton, N. S. (2018) · Physical Chemistry Chemical Physics · doi:10.1039/c8cp04671a · Cited by 33
Sensitivity and entanglement in the avian chemical compass
Zhang, Y., Berman, G. P., & Kais, S. (2014) · Physical Review E · doi:10.1103/physreve.90.042707 · Cited by 32
Magnetic compass orientation by larval Drosophila melanogaster
Dommer, D. H., Gazzolo, P. J., Painter, M. S., & Phillips, J. B. (2008) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2008.02.001 · Cited by 33
“Magnetic compass orientation in birds has been shown to be sensitive to both the wavelength and intensity of light, as well as to low-level radio-frequency fields, both of which are consistent with a radical pair mechanism (Wiltschko and Wiltschko, 1995; Ritz et al., 2000, 2004; Thalau et al., 2004; Muheim et al., 200…”
BackgroundLearned magnetic map cues and two mechanisms of magnetoreception in turtles
Goforth, K. M., Lohmann, C. M. F., Gavin, A. S., Henning, R., Harvey, A., Hinton, T. L., Lim, D. S., & Lohmann, K. J. (2025) · Nature · doi:10.1038/s41586-024-08554-y · Cited by 32
“Among these is the chemical magnetoreception or radical pair hypothesis, which proposes that light-induced chemical reactions enable animals to detect the magnetic field of the Earth 4,32,33 .”
Mouritsen, H. (2013) · Springer eBooks · doi:10.1007/978-3-642-10769-6_20 · Cited by 32
Multiscale description of avian migration: from chemical compass to behaviour modeling
Pedersen, J. B., Nielsen, C., & Solov’yov, I. A. (2016) · Scientific Reports · doi:10.1038/srep36709 · Cited by 32
“(6), calculated for the reaction scheme depicted in Fig.”
BackgroundInfluentialMagnetosensitivity in Dipolarly Coupled Three-Spin Systems
Keens, R. H., Bedkihal, S., & Kattnig, D. R. (2018) · Physical Review Letters · doi:10.1103/physrevlett.121.096001 · Cited by 32
Animal navigation: a noisy magnetic sense?
Johnsen, S., Lohmann, K. J., & Warrant, E. J. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.164921 · Cited by 32
“Photoreceptive proteins known as cryptochromes have been proposed as a possible magnetoreceptive substrate (Ritz et al., 2000). brighter but still coarse image.”
BackgroundSuppression of Arabidopsis flowering by near‐null magnetic field is affected by light
Xu, C., Li, Y., Yu, Y., Zhang, Y., & Wei, S. (2015) · Bioelectromagnetics · doi:10.1002/bem.21927 · Cited by 31
“In magnetoreception research, CRY, first found in Arabidopsis, was suggested to be a magnetoreceptor based on radical-pair mechanism [Ritz et al., 2000].”
BackgroundThe influence of geomagnetic field compensation on human cognitive processes
Sarimov, R. M., Binhi, V. N., & Milyaev, V. A. (2008) · BIOPHYSICS · doi:10.1134/s0006350908050205 · Cited by 32
Procopio, M., Link, J. J., Engle, D., Witczak, J., Ritz, T., & Ahmad, M. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.00888 · Cited by 32
“Intriguingly, the avian cry1a, which is thought to be implicated in sensing of the geomagnetic field (Ritz et al., 2000), also appears to adopt a three-state photocycle wherein the FADH− but not the FADH◦ redox state is the signaling state (Nießner et al., 2013).”
BackgroundSelf-citationTesting the Conjecture That Quantum Processes Create Conscious Experience
Neven, H., Read, P., Kosik, K. S., Van der Molen, T., Bouwmeester, D., Bodnia, E., Turin, L., & Koch, C. (2024) · doi:10.20944/preprints202402.1751.v1 · Cited by 33
“For instance, it has been proposed that this involves a radical pair mechanism, a quantum biological effect that is suspected to underlie bird magnetoreception [34] or lithium’s effects on hyperactivity [35–37].”
BackgroundYukawa, H., Kono, H., Ishiwata, H., Igarashi, R., Takakusagi, Y., Arai, S., Hirano, Y., Suhara, T., & Baba, Y. (2025) · Chemical Society Reviews · doi:10.1039/d4cs00650j · Cited by 35
Tenebrio beetles use magnetic inclination compass
Vácha, M., Drštková, D., & Půžová, T. (2008) · Die Naturwissenschaften · doi:10.1007/s00114-008-0377-9 · Cited by 31
“As far as the mechanism of reception is concerned, such a reaction best corresponds to the radical-pair compass (Ritz et al. 2000) which does not directly detect polarity.”
BackgroundKrapf, S., Koslowski, T., & Steinbrecher, T. B. (2010) · Physical Chemistry Chemical Physics · doi:10.1039/c000876a · Cited by 30
Arabidopsis cryptochrome is responsive to Radiofrequency (RF) electromagnetic fields
Albaqami, M., Hammad, M., Pooam, M., Procopio, M., Sameti, M., Ritz, T., Ahmad, M., & Martino, C. F. (2020) · Scientific Reports · doi:10.1038/s41598-020-67165-5 · Cited by 32
Self-citationMagnetoreception in birds and its use for long-distance migration
Mouritsen, H. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819770-7.00040-2 · Cited by 31
Metadata
- Authors
- Ritz, T., Adem, S., & Schulten, K.
- Affiliations
- University of Illinois Urbana-Champaign (US)
- Corresponding author
- Schulten, Klaus
- Venue
- Biophysical Journal
- Publisher
- Elsevier BV
- Published
- 2000-02
- Volume
- 78
- Issue
- 2
- Pages
- 707-718
- ISSN
- 0006-3495 (ISSN-L)
- PMC
- PMC1300674
- OpenAlex
- W2138668594
- Cited by
- 1,176
- References
- 62
- Citations by year
- 2026: 68 · 2025: 63 · 2024: 49 · 2023: 66 · 2022: 62 · 2021: 71 · 2020: 59 · 2019: 40 · 2018: 58 · 2017: 71 · 2016: 59 · 2015: 46 · 2014: 73 · 2013: 36 · 2012: 42
- FWCI
- 8.03
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biophysical Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Center for Research Resources (P41RR005969)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Electromagnetic Fields and Biological Effects
- Physical Sciences › Earth and Planetary Sciences › Geophysics › Geomagnetism and Paleomagnetism Studies
- Physical Sciences › Chemistry › Spectroscopy › Electron Spin Resonance Studies
- Keywords
- magnetoreception, birds, geomagnetic field, radical pairs, cryptochrome, photoreceptors, hyperfine interaction, magnetic compass, phototransduction, reaction yield
- MeSH terms
- Animals, Birds, Eye Proteins, Flavoproteins, Homing Behavior, Magnetics, Models, Biological, Visual Perception, Anisotropy, Photoreceptor Cells, Invertebrate, Photoreceptor Cells, Vertebrate, Drosophila Proteins, Receptors, G-Protein-Coupled, Cryptochromes
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