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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Quantum biology has been benefitting from refinement of experimental tools that are beginning to provide direct access to observation of quantum dynamics in biological systems.
“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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BackgroundA radical sense of direction: signalling and mechanism in cryptochrome magnetoreception
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Usselman, R. J., Hill, I., Singel, D. J., & Martino, C. F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093065 · Cited by 125 · see citing works
“3 MHz at SMF 45 mT), between O2 N2 and FADH free-radical pairs [16,35,38].”
BackgroundMethodInfluentialFleming, G. R., Scholes, G. D., & Cheng, Y. (2011) · Procedia Chemistry · doi:10.1016/j.proche.2011.08.011 · Cited by 127 · see citing works
Sheppard, A. R., Swicord, M. L., & Balzano, Q. (2008) · Health Physics · doi:10.1097/01.hp.0000319903.20660.37 · Cited by 122 · see citing works
“A broadband magnetic field (0.1 to 10 MHz) at the remarkably low level of 0.085 T, approximately 0.2% the geomagnetic field strength, was sufficient to disrupt orienting behavior attributed to a radical pair mechanism in birds (Ritz et al. 2004).”
BackgroundMethodInfluentialAcuity of a Cryptochrome and Vision-Based Magnetoreception System in Birds
Solov’yov, I. A., Mouritsen, H., & Schulten, K. (2010) · Biophysical Journal · doi:10.1016/j.bpj.2010.03.053 · Cited by 119 · see citing works
Hogben, H. J., Efimova, O., Wagner-Rundell, N., Timmel, C. R., & Hore, P. J. (2009) · Chemical Physics Letters · doi:10.1016/j.cplett.2009.08.051 · Cited by 114 · see citing works
Conservation physiology of animal migration
Lennox, R. J., Chapman, J. M., Souliere, C. M., Tudorache, C., Wikelski, M. C., Metcalfe, J. D., & Cooke, S. J. (2016) · Conservation Physiology · doi:10.1093/conphys/cov072 · Cited by 115 · see citing works
“Migratory movements can be as vast as the transcontinental treks of African wildebeest or as minute as diel vertical migration of zooplankton within metres of the water surface.”
BackgroundQuantum Zeno effect explains magnetic-sensitive radical-ion-pair reactions
Kominis, I. K. (2009) · Physical Review E · doi:10.1103/physreve.80.056115 · Cited by 113 · see citing works
Phillips, J. B., Jorge, P. E., & Muheim, R. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0459.focus · Cited by 110 · see citing works
Self-citationMagnetoreception: activated cryptochrome 1a concurs with magnetic orientation in birds
Nießner, C., Denzau, S., Stapput, K., Ahmad, M., Peichl, L., Wiltschko, W., & Wiltschko, R. (2013) · Journal of The Royal Society Interface · doi:10.1098/rsif.2013.0638 · Cited by 109 · see citing works
“It is generally accepted that in order to provide magnetic directional information, radical pairs must be formed [4,5].”
BackgroundSelf-citationSchwarze, S., Schneider, N.-L., Reichl, T., Dreyer, D., Lefeldt, N., Engels, S., Baker, N., Hore, P. J., & Mouritsen, H. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00055 · Cited by 109 · see citing works
“The lack of electromagnetic screening in these huts means that the Frankfurt birds would inevitably have experienced irregular and unpredictable time-dependent fields resulting from the use of electrical equipment in the adjacent buildings.”
BackgroundResultInfluentialMagnetoreception in birds: two receptors for two different tasks
Wiltschko, W., & Wiltschko, R. (2007) · Journal für Ornithologie · doi:10.1007/s10336-007-0233-2 · Cited by 107 · see citing works
“0-MHz field—were found to be disoriented when these fields were presented at an 24 or 48 angle to the geomagnetic field, but the birds were well oriented when the same fields were presented parallel to the geomagnetic vector (Fig. 11; Ritz et al. 2004; Thalau et al. 2005; Wiltschko et al. 2005).”
BackgroundSelf-citationChemical Compass Model for Avian Magnetoreception as a Quantum Coherent Device
Cai, J., & Plenio, M. B. (2013) · Physical Review Letters · doi:10.1103/physrevlett.111.230503 · Cited by 107 · see citing works
Hochstoeger, T., Said, T. A., Maestre, D., Walter, F., Vilceanu, A., Pedron, M., Cushion, T. D., Snider, W., Nimpf, S., Nordmann, G. C., et al. (2020) · Science Advances · doi:10.1126/sciadv.abb9110 · Cited by 100 · see citing works
Magnetic alignment in mammals and other animals
Begall, S., Malkemper, E. P., Červený, J., Němec, P., & Burda, H. (2012) · Mammalian Biology · doi:10.1016/j.mambio.2012.05.005 · Cited by 105 · see citing works
“Wiltschko andWiltschko, 1972), pulse re-magnetization (Kalmijn and Blakemore, 1978) or exposure to magnetic fields oscillating in the MHz range (Ritz et al., 2004) are available and have been widely used to study mechanisms of magnetic compass orientation.”
BackgroundThe magnetic compass of domestic chickens,Gallus gallus
Wiltschko, W., Freire, R., Munro, U. H., Ritz, T., Rogers, L. J., Thalau, P., & Wiltschko, R. (2007) · Journal of Experimental Biology · doi:10.1242/jeb.004853 · Cited by 99 · see citing works
Self-citationThe magnetic compass mechanisms of birds and rodents are based on different physical principles
Thalau, P., Ritz, T., Burda, H., Wegner, R., & Wiltschko, R. (2006) · Journal of The Royal Society Interface · doi:10.1098/rsif.2006.0130 · Cited by 99 · see citing works
“…broad-band HF field and the 1.315 MHz field of 480 nT, we used the same equipment that we had used in the corresponding experiments with birds (Ritz et al. 2004; Thalau et al. 2005): a coil antenna of a single winding of coaxial cable with 2 cm screening removed opposite the feed was mounted…”
BackgroundMethodInfluentialSelf-citationKirschvink, J. L., Michael Winklhofer, A., & Walker, M. M. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0491.focus · Cited by 96 · see citing works
“Although the spins in the radical pair are not strongly coupled to the thermal bath (Ritz et al. 2004), the proteins that host radical-pair reactions are subject to Brownian motion and therefore must be tethered to larger subcellular components that provide a fixed frame of reference for the compass.”
BackgroundInfluentialPhillips, J. B., Muheim, R., & Jorge, P. E. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.020792 · Cited by 94 · see citing works
“Because cryptochromes do not function as primary visual pigments, and a cryptochrome-based RPM does not require image-forming optics, the LDMC could, in principal, be found in any tissue in the body that receives significant levels of light.”
BackgroundMethodInfluentialSelf-citationThe magnetite-based receptors in the beak of birds and their role in avian navigation
Wiltschko, R., & Wiltschko, W. (2012) · Journal of Comparative Physiology A · doi:10.1007/s00359-012-0769-3 · Cited by 93 · see citing works
“Other types of magnetoreception, like the radical-pair processes in the eye (Ritz et al. 2000, 2004), are not affected by the pulse, however.”
BackgroundSelf-citationTrue navigation in birds: from quantum physics to global migration
Holland, R. A. (2014) · Journal of Zoology · doi:10.1111/jzo.12107 · Cited by 91 · see citing works
Anthropogenic radiofrequency electromagnetic fields as an emerging threat to wildlife orientation
Balmorí, A. (2015) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2015.02.077 · Cited by 90 · see citing works
Pain perception and electromagnetic fields
Seppia, C. D., Ghione, S., Luschi, P., Ossenkopp, K., Choleris, E., & Kavaliers, M. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.01.003 · Cited by 90 · see citing works
Effect of magnetic fields on cryptochrome-dependent responses in Arabidopsis thaliana
Harris, S.-R., Henbest, K. B., Maeda, K., Pannell, J. R., Timmel, C. R., Hore, P. J., & Okamoto, H. (2009) · Journal of The Royal Society Interface · doi:10.1098/rsif.2008.0519 · Cited by 88 · see citing works
“It is difficult to discern a systematic difference in the hypocotyl lengths of the seedlings grown in Oxford, Paris and Frankfurt that might shed light on our failure to replicate the earlier results.”
BackgroundMethodInfluentialLight-dependent magnetoreception in birds: the crucial step occurs in the dark
Wiltschko, R., Ahmad, M., Nießner, C., Gehring, D., & Wiltschko, W. (2016) · Journal of The Royal Society Interface · doi:10.1098/rsif.2015.1010 · Cited by 86 · see citing works
“The model is supported by the observation that radio-frequency fields in the MHz range, a diagnostic tool for radical pair mechanisms [1,2], disrupt magnetic compass orientation of all bird species tested so far [3–8].”
Self-citationMigratory Birds Use Head Scans to Detect the Direction of the Earth's Magnetic Field
Mouritsen, H., Feenders, G., Liedvogel, M., & Kropp, W. (2004) · Current Biology · doi:10.1016/j.cub.2004.10.025 · Cited by 86 · see citing works
Magnetic compass orientation in C57BL/6J mice
Muheim, R., Edgar, N. M., Sloan, K. A., & Phillips, J. B. (2006) · Learning & Behavior · doi:10.3758/bf03193201 · Cited by 87 · see citing works
“…that have been shown to disrupt magnetic compass orientation in organisms with light-dependent [photoreceptor-based?] magnetoreception mechanisms [Ritz et al., 2004] and/or pulse remagnetization that has been shown to affect magnetic responses in organisms with non–light-dependent…”
Self-citationEveraert, J., & Bauwens, D. (2007) · Electromagnetic Biology and Medicine · doi:10.1080/15368370701205693 · Cited by 85 · see citing works
“Several bird species also use magnetic navigation (Liboff and Jenrow, 2000; Muheim et al., 2006) and can become disorientated when exposed to weak ( Ritz et al., 2004; Thalau et al., 2005).”
BackgroundMagnetic field-dependent molecular and chemical processes in biochemistry, genetics and medicine
Buchachenko, A. L. (2014) · Russian Chemical Reviews · doi:10.1070/rc2014v083n01abeh004335 · Cited by 83 · see citing works
Bonadonna, F., Bajzak, C., Benhamou, S., Iglói, K., Jouventin, P., Lipp, H., & Dell’Omo, G. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.2984 · Cited by 83 · see citing works
“We cannot rule out that albatrosses possess an unidentified organ for navigationally relevant magneto-perception in part of their body, such as the caudal parts, more distant than 15 cm from the magnet, although this appears unlikely in view of recent reports of magnetic sensing through the visual system of migratory…”
BackgroundMagnetobiology: The kT Paradox and Possible Solutions
Binhi, V. N., & Rubin, A. B. (2007) · Electromagnetic Biology and Medicine · doi:10.1080/15368370701205677 · Cited by 82 · see citing works
Hiscock, H. G., Mouritsen, H., Manolopoulos, D. E., & Hore, P. J. (2017) · Biophysical Journal · doi:10.1016/j.bpj.2017.07.031 · Cited by 82 · see citing works
“However, it is the disorientation of birds exposed to very weak radiofrequency magnetic fields (1,12) that arguably rules out the competing hypotheses based on superparamagnetic (13) or ferrimagnetic particles (14).”
BackgroundInfluentialRadio frequency magnetic fields disrupt magnetoreception in American cockroach
Vácha, M., Půžová, T., & Kvíčalová, M. (2009) · Journal of Experimental Biology · doi:10.1242/jeb.028670 · Cited by 79 · see citing works
“The RF field was generated, as described by Ritz et al. (Ritz et al., 2004), by the RF generator Stanford Research System DS 34 and amplified with the RF amplifier Research AF Model 25W 1000 (Stanford Research Systems, Sunnyvale, VA, USA).”
BackgroundMethodInfluentialRadical-Pair-Based Magnetoreception Amplified by Radical Scavenging: Resilience to Spin Relaxation
Kattnig, D. R. (2017) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.7b07672 · Cited by 80 · see citing works
Malkemper, E. P., Eder, S. H. K., Begall, S., Phillips, J. B., Michael Winklhofer, A., Hart, V., & Burda, H. (2015) · Scientific Reports · doi:10.1038/srep09917 · Cited by 78 · see citing works
Self-citationMagnetic Strategies for Nervous System Control
Christiansen, M. G., Senko, A. W., & Anikeeva, P. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070918-050241 · Cited by 76 · see citing works
“…compelling form of evidence based on a magnetic stimulus is the use of alternating magnetic fields varied over a wide frequency band in the low MHz to induce transitions between the singlet and triplet states that apparently interfere with magnetosensation (Ritz et al. 2004, Wiltschko et al. 2015).”
BackgroundOrientation of Birds in Total Darkness
Stapput, K., Thalau, P., Wiltschko, R., & Wiltschko, W. (2008) · Current Biology · doi:10.1016/j.cub.2008.03.046 · Cited by 76 · see citing works
Self-citationSensing Magnetic Directions in Birds: Radical Pair Processes Involving Cryptochrome
Wiltschko, R., & Wiltschko, W. (2014) · Biosensors · doi:10.3390/bios4030221 · Cited by 76 · see citing works
Self-citationDogs are sensitive to small variations of the Earth’s magnetic field
Hart, V., Nováková, P., Malkemper, E. P., Begall, S., Hanzal, V., Ježek, M., Kušta, T., Němcová, V., Adámková, J., Benediktová, K., et al. (2013) · Frontiers in Zoology · doi:10.1186/1742-9994-10-80 · Cited by 75 · see citing works
“From the two putative mechanisms that are discussed in birds and other vertebrates (radical-pairs and single-domain or superparamagnetic particles [30,31]) both might account for the observed alignment of the dogs and their sensitivity to declination changes.”
BackgroundDaily repeated magnetic field shielding induces analgesia in CD‐1 mice
Prato, F. S., Robertson, J. A., Desjardins, D., Hensel, J., & Thomas, A. W. (2005) · Bioelectromagnetics · doi:10.1002/bem.20056 · Cited by 75 · see citing works
“The biological transduction mechanisms of magnetoreception in higher order species have been difficult to identify and remain to be conclusively understood [Phillips et al., 2002; Ritz et al., 2002, 2004].”
BackgroundBelyaev, I. Y., Markovà, E., Hillert, L., Malmgren, L. O. G., & Persson, B. (2008) · Bioelectromagnetics · doi:10.1002/bem.20445 · Cited by 74 · see citing works
“Frequency-dependent interactions of MWs with such targets as cellular membranes, chromosomal DNA, radicals, proteins and ions in protein cavities may be involved in effects of MWs [Ismailov, 1987; Belyaev et al., 1992b; Chiabrera et al., 2000; Binhi, 2002; de Pomerai et al., 2003; Ritz et al., 2004].”
BackgroundReaction Kinetics and Mechanism of Magnetic Field Effects in Cryptochrome
Solov’yov, I. A., & Schulten, K. (2011) · The Journal of Physical Chemistry B · doi:10.1021/jp209508y · Cited by 75 · see citing works
Photolyases and cryptochromes: common mechanisms of DNA repair and light-driven signaling?
Essen, L. (2006) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2006.01.004 · Cited by 73 · see citing works
Magnetoreception in birds: the effect of radio-frequency fields
Wiltschko, R., Thalau, P., Gehring, D., Nießner, C., Ritz, T., & Wiltschko, W. (2014) · Journal of The Royal Society Interface · doi:10.1098/rsif.2014.1103 · Cited by 72 · see citing works
“This effect appears to be a specific interference with the magnetoreception process: radio-frequency fields disrupt orientation only if applied at an angle to the magnetic vector; the same fields applied parallel had no effect [9,11].”
BackgroundMethodInfluentialSelf-citation
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › 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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