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Resonance effects indicate a radical-pair mechanism for avian magnetic compass
Abstract
Migratory birds are known to use the geomagnetic field as a source of compass information. There are two competing hypotheses for the primary process underlying the avian magnetic compass, one involving magnetite, the other a magnetically sensitive chemical reaction. Here we show that oscillating magnetic fields disrupt the magnetic orientation behaviour of migratory birds. Robins were disoriented when exposed to a vertically aligned broadband (0.1-10 MHz) or a single-frequency (7-MHz) field in addition to the geomagnetic field. Moreover, in the 7-MHz oscillating field, this effect depended on the angle between the oscillating and the geomagnetic fields. The birds exhibited seasonally appropriate migratory orientation when the oscillating field was parallel to the geomagnetic field, but were disoriented when it was presented at a 24 degrees or 48 degrees angle. These results are consistent with a resonance effect on singlet-triplet transitions and suggest a magnetic compass based on a radical-pair mechanism.
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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 [12]
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BackgroundCould light harvesting complexes exhibit non-classical effects at room temperature?
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Two Different Types of Light-Dependent Responses to Magnetic Fields in Birds
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InfluentialSelf-citationThe Magnetic Compass of Birds: The Role of Cryptochrome
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Self-citationMagnetoreception in microorganisms and fungi
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Oscillating magnetic field disrupts magnetic orientation in Zebra finches, Taeniopygia guttata
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BackgroundCryptochrome 1 in Retinal Cone Photoreceptors Suggests a Novel Functional Role in Mammals
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“…evidence consistent with this hypothesis in birds and newts, suggesting that these animals obtain directional information from a chemically-based magnetic compass (Phillips and Borland 1992; Wiltschko et al. 1993; Wiltschko and Wiltschko 1995b, 1999, 2001; Munro et al. 1997; Ritz et al. 2004).”
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Do magnetic fields cause increased risk of childhood leukemia via melatonin disruption?
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“It has been reported to alter the activities of enzymes which improve the total antioxidative defence capacity of the organism (Rodriguez et al. 2004).”
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Worster, S. B., Kattnig, D. R., & Hore, P. J. (2016) · The Journal of Chemical Physics · doi:10.1063/1.4958624 · Cited by 63
Search for the compass needles
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Avian Navigation: A Combination of Innate and Learned Mechanisms
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“…Falkenberg et al., 2010), putatively acting as a part of a magnetic map ⁄ signpost sense (Mora et al., 2004; Heyers et al., 2010); and (ii) light-dependent radical-pair reactions in the birds’ eyes (Ritz et al., 2000, 2004; Maeda et al., 2008) probably providing directional compass information.”
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“Many different animal species can use geomagnetic cues in the form of a magnetic compass and/or a as magnetic signpost or map sense [18 ,19,20,32,45,60,61 ,62–64].”
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InfluentialSelf-citationPhotoactivation of the cryptochrome/photolyase superfamily
Wang, J., Du, X., Pan, W., Wang, X., & Wu, W. (2014) · Journal of Photochemistry and Photobiology C Photochemistry Reviews · doi:10.1016/j.jphotochemrev.2014.12.001 · Cited by 60
Migratory bats respond to artificial green light with positive phototaxis
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Magnetic Alignment in Carps: Evidence from the Czech Christmas Fish Market
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“[32,33]), is also to be expected at the localities studied.”
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“The first is based on retinal chemo-physical radical-pair reactions (Ritz et al., 2000), a system suggested as the primary signal transduction process for migratory birds (Ritz et al., 2004).”
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Spin-related excited-state phenomena in photochemistry
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ELF magnetic fields: Animal studies, mechanisms of action
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“…indeed disrupted magnetic orientation of European robins, Erithacus rubecula (Turdidae), domestic chickens, Gallus gallus (Phasianidae), and zebra finches, Taeniopygia guttata (Estrildidae) (Ritz et al., 2004; Ritz et al., 2009; Thalau et al., 2005; Wiltschko et al., 2007; Keary et al., 2009).”
BackgroundSelf-citationNight-Migratory Songbirds Possess a Magnetic Compass in Both Eyes
Engels, S., Hein, C. M., Lefeldt, N., Prior, H., & Mouritsen, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043271 · Cited by 52
“The direction of the Earth’s magnetic field is supposedly sensed by radical pair-forming, light-dependent photopigments in the birds eyes [4,11–20] and then processed in Cluster N, a specialized, night-time active, light-processing forebrain region [9,21–24] which is required for magnetic compass orientation [10].”
BackgroundNo evidence for magnetic field effects on the behaviour of Drosophila
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Magnetic orientation of garden warblers ( Sylvia borin ) under 1.4 MHz radiofrequency magnetic field
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Bird navigation: what type of information does the magnetite-based receptor provide?
Wiltschko, W., Munro, U. H., FORD, H. A., & Wiltschko, R. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3651 · Cited by 52
“Recent experiments in high-frequency fields directly indicated an underlying radical pair mechanism (Ritz et al. 2004; Thalau et al. 2005; Wiltschko et al. 2005).”
BackgroundSelf-citationDifferential effects of magnetic pulses on the orientation of naturally migrating birds
Holland, R. A. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2010.0159 · Cited by 52
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Avian orientation: the pulse effect is mediated by the magnetite receptors in the upper beak
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“The inclination compass thus works independently of the magnetite-based receptors; it appears to be entirely based on radical-pair processes in the eye (Wiltschko, W. et al. 2002; Ritz et al. 2004; Thalau et al. 2005), with the respective information mediated by the optical nerve.”
BackgroundSelf-citationPolarized light modulates light-dependent magnetic compass orientation in birds
Muheim, R., Sjöberg, S., & Pinzon-Rodriguez, A. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1513391113 · Cited by 50
“1–10 MHz (intensity <1 μT) is the most powerful tool to test for an involvement of a radical-pair mechanism in the primary magnetoreception process (19, 34).”
BackgroundMethodResultMagnetoreception in birds: Different physical processes for two types of directional responses
Wiltschko, R., Stapput, K., Ritz, T., Thalau, P., & Wiltschko, W. (2007) · HFSP journal · doi:10.2976/1.2714294 · Cited by 50
Self-citationNon-thermal effects and mechanisms of interaction between electromagnetic fields and living matter
Giuliani, L., & Soffritti, M. (2010) · Cited by 50
Zebra finches have a light-dependent magnetic compass similar to migratory birds
Pinzon-Rodriguez, A., & Muheim, R. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.148098 · Cited by 49
“…which is a diagnostic test to assess the involvement of a radical pair mechanism in the primary magnetoreception process (Timmel and Hore, 1996; Ritz et al., 2004; Henbest et al., 2004), zebra finches were no longer able to use their magnetic compass (Keary et al., 2009; Muheim et al., 2016).”
BackgroundInfluentialNontrivial quantum and quantum-like effects in biosystems: Unsolved questions and paradoxes
Melkikh, A. V., & Khrennikov, A. Y. (2015) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2015.07.001 · Cited by 49
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Condensed Matter Systems Exposed to Radiation: Multiscale Theory, Simulations, and Experiment
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THE MANY FACES OF ORGANIC MAGNETORESISTANCE
Wagemans, W., JANSSEN, P., Schellekens, A. J., BLOOM, F. L., Bobbert, P. A., & Koopmans, B. (2011) · SPIN · doi:10.1142/s2010324711000082 · Cited by 48
A light-dependent magnetoreception mechanism insensitive to light intensity and polarization
Worster, S. B., Mouritsen, H., & Hore, P. J. (2017) · Journal of The Royal Society Interface · doi:10.1098/rsif.2017.0405 · Cited by 46
Bolte, P., Einwich, A., Seth, P. K., Chetverikova, R., Heyers, D., Wojahn, I., Janssen‐Bienhold, U., Feederle, R., Hore, P. J., Dedek, K., et al. (2021) · Ethology Ecology & Evolution · doi:10.1080/03949370.2020.1870571 · Cited by 48
“Magnetic orientation in night-migratory songbirds is light-dependent (Wiltschko et al. 1993, 2010) and sensitive to radiofrequency magnetic fields (Ritz et al. 2004; Engels et al. 2014; Schwarze et al. 2016; Kobylkov et al. 2020).”
BackgroundLight-dependent magnetoreception: orientation behaviour of migratory birds under dim red light
Wiltschko, R., Munro, U. H., FORD, H. A., Stapput, K., & Wiltschko, W. (2008) · Journal of Experimental Biology · doi:10.1242/jeb.020313 · Cited by 48
“, 2003b), with the respective directional information mediated by radical pair processes (Ritz et al., 2004; Thalau et al., 2005).”
BackgroundSelf-citationHow quantum is radical pair magnetoreception?
Fay, T. P., Lindoy, L. P., Manolopoulos, D. E., & Hore, P. J. (2020) · Faraday Discussions · doi:10.1039/c9fd00049f · Cited by 47
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The puzzle of magnetic resonance effect on the magnetic compass of migratory birds
Kavokin, K. V. (2009) · Bioelectromagnetics · doi:10.1002/bem.20485 · Cited by 47
“As our analysis has shown, the radical pair model is unable to explain the results of the experiments [Ritz et al 2004, Thalau et al 2005, Stapput et al 2006, Wiltschko et al 2007] on disruption of the bird magnetic compass by radio-frequency magnetic fields.”
BackgroundResultInfluentialThe use of the geomagnetic field for short distance orientation in zebra finches
Voss, J., Keary, N., & Bischof, H. (2007) · Neuroreport · doi:10.1097/wnr.0b013e32818b2a21 · Cited by 47
“This is supported by evidence from experiments with other bird species [17].”
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“Several previous studies of the effects of RF fields on magnetic compass orientation have resulted in seemingly contradictory findings ([29,31,33], but see [35]).”
BackgroundResultInfluentialCould light harvesting complexes exhibit non-classical effects at room temperature?
Wilde, M. M., McCracken, J. M., & Mizel, A. (2010) · Civil War Book Review · Cited by 47
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“Previous experiments with migratory birds have shown that exposure to a RF field at the Larmor frequency at intensities as low as 15 nT can abolish magnetic compass orientation [61].”
BackgroundResultInfluentialSelf-citationRapid Learning of Magnetic Compass Direction by C57BL/6 Mice in a 4-Armed ‘Plus’ Water Maze
Phillips, J. B., Youmans, P. W., Muheim, R., Sloan, K. A., Landler, L., Painter, M. S., & Anderson, C. R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073112 · Cited by 46
“Studies of birds and cockroaches suggest that responses to earthstrength (~50 μT) magnetic fields can be disrupted by radio frequency fields tuned to the Larmor Frequency (the precession frequency of the electron spin dipole in the ambient magnetic field) at intensities as low as 10-15 nT [38,39,77,78].”
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Cryptochrome: A photoreceptor with the properties of a magnetoreceptor?
Ritz, T., Yoshii, T., Foerster, C., & Ahmad, M. (2010) · Communicative & Integrative Biology · doi:10.4161/cib.3.1.9865 · Cited by 45
Self-citationRemoval 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
“In the following, we probe the effect of detuning oMW oL in equation (1), the result of which is sketched in Fig.”
InfluentialMyklatun, 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
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
“Migratory birds are prevented from using their magnetic compass by extraordinarily weak broadband radiofrequency noise (Ritz et al., 2009; Ritz et al., 2004; Thalau et al., 2005; Winklhofer et al., 2013; Engels et al., 2014; Kavokin et al., 2014; Wiltschko et al., 2015; Schwarze et al., 2016) the predicted effects of…”
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
“Although evidence consistent with this hypothesis has been acquired in some animals, especially in insects and birds (e.g., Ritz et al. 2004; Gegear et al. 2008; Wan et al. 2021; Netušil et al. 2021), the idea has received little attention in fishes.”
ResultChetverikova, 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
Quantum 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
Magnetic field effects in proteins
Jones, A. R. (2016) · Molecular Physics · doi:10.1080/00268976.2016.1149631 · Cited by 42
Concepts in the Brain: The View From Cross-linguistic Diversity
Kemmerer, D. (2019) · doi:10.1093/oso/9780190682620.001.0001 · 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
“For birds, this model is now supported by experimental evidence demonstrating the involvement of radical pair mechanisms [2-4] and identifying the right eye as site of magnetoreception [5].”
MethodSelf-citationMiura, 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
Avian 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].”
BackgroundMethodSelf-citationThe 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
“Among these sources and hypotheses, magnetite as well as biochemical radical-pair reactions has been hypothesized to mediate sensitivity to Earthstrength magnetic fields through fundamentally different physical mechanisms [68, 69].”
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
“Meanwhile, a recent observation provides strong support for the role of electron spins: the birds are disorientated by a weak oscillatory field whose frequency is close to the resonant frequency for an electron in the Earth’s magnetic field (8,11).”
BackgroundChernetsov, N. (2017) · Journal of Comparative Physiology A · doi:10.1007/s00359-016-1140-x · Cited by 39
“1993, 2000, 2001a; Wiltschko and Wiltschko 2001) and it is disrupted by radiofrequency oscillating magnetic fields (Ritz et al. 2004; Thalau et al. 2005; Kavokin et al. 2014; Engels et al. 2014; but see Schwarze et al. 2016a).”
BackgroundHeams, T. (2014) · Mathematical Structures in Computer Science · doi:10.1017/s096012951200076x · Cited by 42
“Quantum-assisted magnetic sensing has also been suggested as a possible mechanism explaining how migrating birds orient themselves (Ritz et al. 2004; Maeda et al. 2008).”
BackgroundNeurobiology of the homing pigeon—a review
Mehlhorn, J., & Rehkämper, G. (2009) · Die Naturwissenschaften · doi:10.1007/s00114-009-0560-7 · Cited by 40
“Thus, this magnetoreceptor system is light independent and could also be used in the absence of light and other abnormal light regimes (Wiltschko et al. 2002; Ritz et al. 2004; Stapput et al. 2008).”
BackgroundDellis, A. T., & Kominis, I. K. (2011) · Biosystems · doi:10.1016/j.biosystems.2011.11.007 · Cited by 38
“…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 et al., 2009).”
MethodCan 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
Self-citationWiltschko, R., & Wiltschko, W. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-1704-0_8 · Cited by 39
Self-citationENVIRONMENTAL CONDITIONS AFFECT THE BEHAVIOR OF CAPTIVE, MIGRATORY WHITE-CROWNED SPARROWS
Ramenofsky, M., Agatsuma, R., & Ramfar, T. (2008) · Ornithological Applications · doi:10.1525/cond.2008.8523 · Cited by 38
“…compass orientation is known to be a low-level light-dependent process that includes a radical-pair mechanism in Garden Warblers as well as an iron-containing receptor in the upper beak of European Robins (Erithacus rubecula; Ritz et al. 2004, Wiltschko and Wiltschko 2007, Stapput et al. 2008).”
BackgroundMagnetoreception systems in birds: A review of current research
Kishkinev, D., & Chernetsov, N. (2015) · Biology Bulletin Reviews · doi:10.1134/s2079086415010041 · Cited by 36
Building science and radiofrequency radiation: What makes smart and healthy buildings
Clegg, F. M., Sears, M., Friesen, M., Scarato, T., Metzinger, R., Russell, C., Stadtner, A., & Miller, A. B. (2019) · Building and Environment · doi:10.1016/j.buildenv.2019.106324 · Cited by 37
Okano, H., Masuda, H., & Ohkubo, C. (2005) · Bioelectromagnetics · doi:10.1002/bem.20055 · Cited by 37
“…magnetically sensitive physicochemical reactions [Harkins and Grissom, 1994; Grissom, 1995; Eichwald and Walleczek, 1996; Weaver et al., 2000; Ritz et al., 2000, 2004] nor the presence of biogenic magnetite (Fe3O4) [Kirschvink and Gould, 1981; Kirschvink et al., 1992, 2001] in some organs,…”
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
“…as a control condition in all our orientation studies since 2001 with light of various wavelengths (see Wiltschko et al., 2010), in the experiments with radio frequency fields (e.g. Ritz et al., 2004; Ritz et al., 2009) and in those on lateralization (Wiltschko et al., 2002; Gehring et al., 2012).”
Self-citationBinhi, V. N. (2005) · Bioelectromagnetics · doi:10.1002/bem.20178 · Cited by 35
“Recent works [Ritz et al., 2004; Thalau et al., 2005] discuss experimental evidence that radical-pair mechanism may underlie the magnetic navigation of migratory birds.”
Background
Metadata
- Authors
- Ritz, T., Thalau, P., Phillips, J. B., Wiltschko, R., & Wiltschko, W.
- Affiliations
- University of California, Irvine (US)
- Goethe University Frankfurt (DE)
- Virginia Tech (US)
- Corresponding author
- Ritz, Thorsten
- Venue
- Nature
- Published
- 2004-05
- Volume
- 429
- Issue
- 6988
- Pages
- 177-180
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1999373473
- Cited by
- 617
- References
- 30
- Citations by year
- 2026: 22 · 2025: 30 · 2024: 18 · 2023: 35 · 2022: 24 · 2021: 20 · 2020: 23 · 2019: 27 · 2018: 20 · 2017: 33 · 2016: 37 · 2015: 26 · 2014: 52 · 2013: 27 · 2012: 28
- FWCI
- 18.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- 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 › Environmental Science › Ecology › Avian ecology and behavior
- Keywords
- radical pair mechanism, migratory birds, geomagnetic field, alternating magnetic field, magnetite, singlet-triplet transitions, magnetic resonance, robins, magnetic orientation, seasonal migration, disorientation
- MeSH terms
- Animals, Europe, Geography, Iron, Magnetics, Models, Biological, Oxides, Songbirds, Animal Migration, Ferrosoferric Oxide
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