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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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From Vibrations, quanta and biology (2013) · cites this paper as [12]
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“Top centre: further evidence supporting a radical pair based magnetic compass comes from the observation that weak radiofrequency magnetic fields seem to disrupt the ability of birds to orient by the Earth's magnetic field (Ritz et al. 2004, 2009, 2010; Thalau et al. 2005).”
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“Data from migratory robins and directionally trained chickens as well as zebra finches show that this is the case (Ritz et al. 2004, 2009; Thalau et al. 2005; Wiltschko, W. et al. 2007; Keary et al. in press), which indicates that the avian magnetic compass is indeed based on a radical-pair…”
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“In migratory birds, recent evidence strongly supports a radical pair mechanism underlying the detection of the geomagnetic Weld (Ritz et al. 2004; Thalau et al. 2005; Wiltschko et al. 2005); this Wnding, combined with the above mentioned evidence implicating a role of cryptochromes (Möller et al.…”
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BackgroundSelf-citationMagnetic compass orientation of migratory birds in the presence of a 1.315�MHz oscillating field
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Self-citationThe magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds
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Direct Observation of a Photoinduced Radical Pair in a Cryptochrome Blue‐Light Photoreceptor
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Self-citationThe Quantum Biology of Reactive Oxygen Species Partitioning Impacts Cellular Bioenergetics
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“This hypothesis is supported by the observations that magnetic compass orientation of migratory birds can be disrupted by weak radiofrequency magnetic fields with frequencies in the 1- to 10-MHz range (21, 24) and that magnetoreception depends on the wavelength of the ambient light (25).”
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BackgroundA radical sense of direction: signalling and mechanism in cryptochrome magnetoreception
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“3 MHz at SMF 45 mT), between O2 N2 and FADH free-radical pairs [16,35,38].”
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Self-citationMagnetoreception: activated cryptochrome 1a concurs with magnetic orientation in birds
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“It is generally accepted that in order to provide magnetic directional information, radical pairs must be formed [4,5].”
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“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
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“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).”
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“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
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
“…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., Winklhofer, M., & Walker, M. M. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0491.focus · Cited by 100
“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
“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
“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 93
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
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
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
“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
“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
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
“…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
“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
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
“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
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
“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
“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
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
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 79
“…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
Self-citationSensing Magnetic Directions in Birds: Radical Pair Processes Involving Cryptochrome
Wiltschko, R., & Wiltschko, W. (2014) · Biosensors · doi:10.3390/bios4030221 · Cited by 76
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 83
“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
“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
“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
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
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
“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
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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