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Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird
Abstract
Electromagnetic noise is emitted everywhere humans use electronic devices. For decades, it has been hotly debated whether man-made electric and magnetic fields affect biological processes, including human health. So far, no putative effect of anthropogenic electromagnetic noise at intensities below the guidelines adopted by the World Health Organization has withstood the test of independent replication under truly blinded experimental conditions. No effect has therefore been widely accepted as scientifically proven. Here we show that migratory birds are unable to use their magnetic compass in the presence of urban electromagnetic noise. When European robins, Erithacus rubecula, were exposed to the background electromagnetic noise present in unscreened wooden huts at the University of Oldenburg campus, they could not orient using their magnetic compass. Their magnetic orientation capabilities reappeared in electrically grounded, aluminium-screened huts, which attenuated electromagnetic noise in the frequency range from 50 kHz to 5 MHz by approximately two orders of magnitude. When the grounding was removed or when broadband electromagnetic noise was deliberately generated inside the screened and grounded huts, the birds again lost their magnetic orientation capabilities. The disruptive effect of radiofrequency electromagnetic fields is not confined to a narrow frequency band and birds tested far from sources of electromagnetic noise required no screening to orient with their magnetic compass. These fully double-blinded tests document a reproducible effect of anthropogenic electromagnetic noise on the behaviour of an intact vertebrate.
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“It is the singlet -triplet mixing that experiences the influence of the Earth's magnetic field and that has offered some way of explaining behavioural observations such as the light-dependence [94], inclination aspect [95] and resonance effects of the avian compass [96,97].”
From The future of quantum biology (2018) · cites this paper as [97]
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“Since cryptochromes are molecules highly sensitive to RF radiation and are found in many organisms, including humans, these results also may have more general implications for the capacity of living organisms to respond to man-made electromagnetic noise by analogy with broadband RF, which has previously been shown to…”
BackgroundKerpal, C., Richert, S., Storey, J. G., Pillai, S., Liddell, P. A., Gust, D., Mackenzie, S. R., Hore, P. J., & Timmel, C. R. (2019) · Nature Communications · doi:10.1038/s41467-019-11655-2 · Cited by 60
Self-citationNoise Reduces Foraging Efficiency in Pallid Bats ( Antrozous pallidus )
Bunkley, J. P., & Barber, J. R. (2015) · Ethology · doi:10.1111/eth.12428 · Cited by 57
A physical mechanism of magnetoreception: Extension and analysis
Binhi, V. N., & Prato, F. S. (2016) · Bioelectromagnetics · doi:10.1002/bem.22011 · Cited by 57
“It is now well established that very weak MFs that may still cause a biological effect are certainly far below levels needed to elicit induced currents that would not be lost in the thermal noise of warm and wet biological systems [Prato et al., 2013; Engels et al., 2014].”
Bird collisions at an offshore platform in the North Sea
Hüppop, O., Hüppop, K., Dierschke, J., & Hill, R. (2016) · Bird Study · doi:10.1080/00063657.2015.1134440 · Cited by 54
“2008) and to put their results into action; (3) to develop a need based beaconing system which will automatically switch on obstruction lights only in case of an approaching watercraft or aircraft; (4) to minimize electromagnetic noise that can disrupt the magnetic compass orientation and lead to disorientation of bir…”
BackgroundLevitt, B. B., Lai, H. C., & Manville, A. M. (2021) · Reviews on Environmental Health · doi:10.1515/reveh-2021-0026 · Cited by 57
“Other uninvestigated research that could have applied included in-fi eld RFR behavioral studies [17, 242]; mortality [134, 243, 244]; reproductive outcomes [16, 18]; and bat insect foraging [36] in the presence of radar.”
BackgroundIdentifying Cellular and Molecular Mechanisms for Magnetosensation
Clites, B. L., & Pierce-Shimomura, J. T. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031312 · Cited by 53
Form and Function of the Vertebrate and Invertebrate Blood-Brain Barriers
Dunton, A. D., Göpel, T., Ho, D. H., & Burggren, W. W. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212111 · Cited by 55
“For example, we may speculate that the BBB plays an important role in bird navigation given that electromagnetic fields (EMF) have been shown to affect mammalian BBB function [120–123] and that EMFs disrupt birds’ magnetic compass [124].”
BackgroundNo evidence for magnetic field effects on the behaviour of Drosophila
Bassetto, M., Reichl, T., Kobylkov, D., Kattnig, D. R., Michael Winklhofer, A., Hore, P. J., & Mouritsen, H. (2023) · Nature · doi:10.1038/s41586-023-06397-7 · Cited by 53
Self-citationMagnetic map navigation in a migratory songbird requires trigeminal input
Pakhomov, A. Y., Анашина, А., Heyers, D., Kobylkov, D., Mouritsen, H., & Chernetsov, N. (2018) · Scientific Reports · doi:10.1038/s41598-018-30477-8 · Cited by 52
Self-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
Fan, X., Ding, H., Li, S., Sanzari, M., Zhang, Y., Trappe, W. K., Han, Z., & Howard, R. E. (2018) · Proceedings of the ACM on Interactive Mobile Wearable and Ubiquitous Technologies · doi:10.1145/3214268 · Cited by 49
“2 WPT Energy Density Distributions and their Implications on Safety The risks of excessive RF energy exposure have been studied in the past, which have revealed that harmful biological effects may stem from strong RF radiation [21, 24, 31, 36, 47, 48].”
BackgroundA 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
Self-citationChallenges of Learning to Escape Evolutionary Traps
Greggor, A. L., Trimmer, P. C., Barrett, B. J., & Sih, A. (2019) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2019.00408 · Cited by 48
“…interference with existing cues, rather than changes to the cue themselves (e.g., electromagnetic noise disrupting migrating birds’ magnetic compass, Engels et al., 2014) are only likely to be alleviated by removal of the interference, since it can be a challenge for animals to set-shift to a new…”
BackgroundBolte, 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
“Thus, the geomagnetic field can influence the proportions of singlet and triplet reaction yields, which in turn can function as a chemical compass (Schulten et al. 1978; Ritz et al. 2000, 2009; Solov’yov et al. 2010, 2014; Mouritsen & Hore 2012; Engels et al. 2014; Hore & Mouritsen 2016).”
BackgroundInfluentialSelf-citationLeberecht, B., Wong, S. Y., Satish, B., Döge, S., Hindman, J., Venkatraman, L., Apte, S., Haase, K., Musielak, I., Dautaj, G., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2301153120 · Cited by 47
Self-citationBreus, T. K., Binhi, V. N., & Petrukovich, A. A. (2016) · Physics-Uspekhi · doi:10.3367/ufne.2015.12.037693 · Cited by 47
Kobylkov, D., Wynn, J., Michael Winklhofer, A., Chetverikova, R., Xu, J., Hiscock, H. G., Hore, P. J., & Mouritsen, H. (2019) · Journal of The Royal Society Interface · doi:10.1098/rsif.2019.0716 · Cited by 47
“We recorded the maxhold signal per squareroot-bandwidth with the ‘Maxpeak’ detector (in keeping with [34]) and the average signal per square-root-bandwidth with the ‘RMS’ detector.”
BackgroundMethodInfluentialSelf-citationLandler, L., Painter, M. S., Youmans, P. W., Hopkins, W. A., & Phillips, J. B. (2015) · PLoS ONE · doi:10.1371/journal.pone.0124728 · Cited by 46
“Recent findings suggest that the threshold of sensitivity of a RPM based system may be as low as 1 nT (RF intensity), which can be in the range of anthropogenic electromagnetic noise [42].”
BackgroundMagnetic field-driven induction of ZENK in the trigeminal system of pigeons ( Columba livia )
Lefeldt, N., Heyers, D., Schneider, N.-L., Engels, S., Elbers, D., & Mouritsen, H. (2014) · Journal of The Royal Society Interface · doi:10.1098/rsif.2014.0777 · Cited by 46
“The testing cabin was lined with aluminium shields and grounded to act as a Faraday cage which shielded time-dependent electromagnetic disturbances with frequencies up to at least 20 MHz by about two orders of magnitude while leaving static fields unaffected [52].”
MethodSelf-citationPrecision apiculture: Development of a wireless sensor network for honeybee hives
Henry, E., Adamchuk, V. I., Stanhope, T. P., Buddle, C. M., & Rindlaub, N. (2018) · Computers and Electronics in Agriculture · doi:10.1016/j.compag.2018.11.001 · Cited by 46
“In migratory robins, which possess identical magnetite-based navigation systems to honeybees, RF-EMR affect navigation (Engels et al., 2014).”
BackgroundChallenges in coupling atmospheric electricity with biological systems
Hunting, E. R., Matthews, J. C., Fdez-Arróyabe, P., England, S. J., Kourtidis, K., Koh, K. L., Nicoll, K., Harrison, R. G., Manser, K., Price, C. G., et al. (2020) · International Journal of Biometeorology · doi:10.1007/s00484-020-01960-7 · Cited by 46
Cryptochromes: Photochemical and structural insight into magnetoreception
Karki, N., Vergish, S., & Zoltowski, B. D. (2021) · Protein Science · doi:10.1002/pro.4124 · Cited by 49
“Notably, quantum mechanical calculations suggest that the spin dynamics of the superoxide radical are incompatible with the RPhypothesis(52) and in vivo data exists that contradicts a dark-dependent radical pair.(53,54) The RP-model was complicated by initial studies of CRY proteins that questioned a Trp-triad based m…”
BackgroundConservation Strategies for Bats Flying at High Altitudes
Voigt, C. C., Currie, S. E., Fritze, M., Roeleke, M., & Lindecke, O. (2018) · BioScience · doi:10.1093/biosci/biy040 · Cited by 44
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
Self-citationVery 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 649 prevented from using their magnetic compass by extraordinarily weak broadband 650 radiofrequency noise (60, 110-116) the predicted effects of which are far too small to be 651 consistent with our current understanding of radical pair spin dynamics (117, 118).”
BackgroundSelf-citation
Metadata
- Authors
- Engels, S., Schneider, N.-L., Lefeldt, N., Hein, C. M., Zapka, M., Michalik, A., Elbers, D., Kittel, A., Hore, P. J., & Mouritsen, H.
- Affiliations
- Carl von Ossietzky Universität Oldenburg (DE)
- University of Oxford (GB)
- Corresponding author
- Mouritsen, Henrik
- Venue
- Nature
- Published
- 2014-05
- Volume
- 509
- Issue
- 7500
- Pages
- 353-356
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2155559532
- Cited by
- 403
- References
- 36
- Citations by year
- 2026: 29 · 2025: 32 · 2024: 22 · 2023: 38 · 2022: 45 · 2021: 36 · 2020: 34 · 2019: 30 · 2018: 32 · 2017: 32 · 2016: 32 · 2015: 26 · 2014: 15
- FWCI
- 20.77
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- 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
- magnetic compass orientation, magnetic orientation, European robin, Erithacus rubecula, bird migration, geomagnetic field, electromagnetic interference shielding, grounding, bioelectromagnetics, songbirds, urbanization effects on wildlife
- MeSH terms
- Aluminum, Animals, Cities, Conservation of Natural Resources, Double-Blind Method, Electricity, Electromagnetic Fields, Electronics, Germany, Housing, Orientation, Radio Waves, Seasons, Universities, Reproducibility of Results, Songbirds, Animal Migration, Magnetic Fields
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