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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Singlet-triplet mixing experiences the influence of the Earth's magnetic field and has offered some way of explaining behavioural observations such as light-dependence, inclination aspect and resonance effects of the avian compass.
“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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“broadband electromagnetic noise containing a range of radiofrequencies (17,18).”
BackgroundInfluentialSelf-citationRadical-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
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“These field strengths are comparable to the ones used in Engels et al.(39), who were able to disrupt the magnetic compass orientation of European robins by broadband electromagnetic noise with a spectral intensity of 0.”
BackgroundResultInfluentialQuantum effects in the brain: A review
Adams, B., & Petruccione, F. (2020) · AVS Quantum Science · doi:10.1116/1.5135170 · Cited by 80 · see citing works
Magnetic 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
“…strikes at very close range (Fuchset et al. 1998) or weak electromagnetic signals linked to human technology or solar wind (LaBelle & Treumann 2002, Engels et al. 2014), the geomagnetic field seems to be the principal magnetic stimulus of evolutionary significance to animals in their natural…”
BackgroundInteractions between electromagnetic radiation and biological systems
Liu, L., Huang, B., Lu, Y., Zhao, Y., Tang, X., & Shi, Y. (2024) · iScience · doi:10.1016/j.isci.2024.109201 · Cited by 80 · see citing works
Sensing 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
Kahle, L. Q., Flannery, M., & Dumbacher, J. P. (2016) · PLoS ONE · doi:10.1371/journal.pone.0144600 · Cited by 76 · see citing works
“In contrast, in urban settings with minimal or no surrounding vegetation [25] and only a few urban-adapted seasonal residents, the majority of strikes may occur during migration periods, when disoriented migrant birds lose their way in the urban or suburban cityscape with taller buildings that are illuminated at night…”
BackgroundInternational Commission on the Biological Effects of Electromagnetic Fields (ICBE-EMF), Belyaev, I. Y., Blackman, C. F., Chamberlin, K. A., DeSalles, A., Daşdağ, S., Fernández, C., Hardell, L., Héroux, P., Kelley, E., et al. (2022) · Environmental Health · doi:10.1186/s12940-022-00900-9 · Cited by 74 · 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
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Natal imprinting to the Earth’s magnetic field in a pelagic seabird
Wynn, J., Padget, O., Mouritsen, H., Perrins, C. M., & Guilford, T. (2020) · Current Biology · doi:10.1016/j.cub.2020.05.039 · Cited by 71 · see citing works
Self-citationViability of superoxide-containing radical pairs as magnetoreceptors
Player, T. C., & Hore, P. J. (2019) · The Journal of Chemical Physics · doi:10.1063/1.5129608 · Cited by 69 · see citing works
Self-citationStructural effects in a composite nonwoven fabric on EMI shielding
Lu, L., Xing, D., Teh, K. S., Liu, H., Xie, Y., Liu, X., & Tang, Y. Z. (2017) · Materials & Design · doi:10.1016/j.matdes.2017.02.025 · Cited by 68 · see citing works
Exploiting common senses: sensory ecology meets wildlife conservation and management
Elmer, L. K., Madliger, C. L., Blumstein, D. T., Elvidge, C. K., Fernández‐Juricic, E., Horodysky, A. Z., Johnson, N. S., McGuire, L. P., Swaisgood, R. R., & Cooke, S. J. (2021) · Conservation Physiology · doi:10.1093/conphys/coab002 · Cited by 66 · see citing works
“Electromagnetic noise from human activity has been shown to disrupt magnetic compass orientation in European robins (Erithacus rubecula) in both natural and labortary settings (Engels et al., 2014; Schwarze et al., 2016).”
BackgroundLevitt, B. B., Lai, H. C., & Manville, A. M. (2021) · Reviews on Environmental Health · doi:10.1515/reveh-2021-0050 · Cited by 65 · see citing works
Spin relaxation of radicals in cryptochrome and its role in avian magnetoreception
Worster, S. B., Kattnig, D. R., & Hore, P. J. (2016) · The Journal of Chemical Physics · doi:10.1063/1.4958624 · Cited by 63 · see citing works
Self-citationAvian Navigation: A Combination of Innate and Learned Mechanisms
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Idumah, C. I., Obele, C. M., & Enwerem, U. E. (2021) · Current Research in Green and Sustainable Chemistry · doi:10.1016/j.crgsc.2021.100104 · Cited by 61 · see citing works
RetractedTheoretical Concepts in Magnetobiology after 40 Years of Research
Binhi, V. N., & Rubin, A. B. (2022) · Cells · doi:10.3390/cells11020274 · Cited by 61 · see citing works
“MF inhomogeneity inside 21 studied incubators for biological research in [55] averaged about 30 and reached hundreds of μT per 10 cm, which is often overlooked in studies of magnetobiology [56], although it is known [34,57,58] that some animals are sensitive to MF changes of 15 to 30 nT.”
BackgroundLeberecht, B., Kobylkov, D., Karwinkel, T., Döge, S., Burnus, L., Wong, S. Y., Apte, S., Haase, K., Musielak, I., Chetverikova, R., et al. (2022) · Journal of Comparative Physiology A · doi:10.1007/s00359-021-01537-8 · Cited by 61 · see citing works
Self-citationMagnetocarcinogenesis: is there a mechanism for carcinogenic effects of weak magnetic fields?
Juutilainen, J., Herrala, M., Luukkonen, J., Naarala, J., & Hore, P. J. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2018.0590 · Cited by 62 · see citing works
Self-citationElectromagnetic radiation as an emerging driver factor for the decline of insects
Balmorí, A. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.144913 · Cited by 61 · see citing works
“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 · see citing works
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 · see citing works
A physical mechanism of magnetoreception: Extension and analysis
Binhi, V. N., & Prato, F. S. (2016) · Bioelectromagnetics · doi:10.1002/bem.22011 · Cited by 57 · see citing works
“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 · see citing works
“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 54 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
“…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 · see citing works
“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 · see citing works
Self-citationBreus, T. K., Binhi, V. N., & Petrukovich, A. A. (2016) · Physics-Uspekhi · doi:10.3367/ufne.2015.12.037693 · Cited by 47 · see citing works
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 · see citing works
“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 · see citing works
“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 · see citing works
“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 · see citing works
“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 · see citing works
Cryptochromes: Photochemical and structural insight into magnetoreception
Karki, N., Vergish, S., & Zoltowski, B. D. (2021) · Protein Science · doi:10.1002/pro.4124 · Cited by 45 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“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
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › 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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