Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird (original) (raw)

Nature volume 509, pages 353–356 (2014)Cite this article

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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 health1,2,[3](/articles/nature13290#ref-CR3 "World Health Organization. Extremely Low Frequency Fields. Environmental Health Criteria Monograph no. 238,. http://www.who.int/peh-emf/publications/elf_ehc/en/

             (2007)"),[4](/articles/nature13290#ref-CR4 "Health Protection Agency. Health Effects from Radiofrequency Electromagnetic Fields. 
              http://www.hpa.org.uk/webc/HPAwebFile/HPAweb_C/1317133827077
              
             (2012)"),[5](/articles/nature13290#ref-CR5 "The INTERPHONE Study Group Brain tumour risk in relation to mobile telephone use: results of the INTERPHONE international case–control study. Int. J. Epidemiol. 39, 675–694 (2010)"). So far, no putative effect of anthropogenic electromagnetic noise at intensities below the guidelines adopted by the World Health Organization[1](/articles/nature13290#ref-CR1 "International Commission for Non-Ionizing Radiation Protection. ICNIRP guidelines for limiting exposure to time-varying electric, magnetic, and electromagnetic fields (up to 300 GHz). Health Phys. 74, 494–522 (1998)"),[2](/articles/nature13290#ref-CR2 "International Commission for Non-Ionizing Radiation Protection. ICNIRP statement on the “Guidelines for limiting exposure to time-varying electric, magnetic, and electromagnetic fields (up to 300 GHz)”. Health Phys. 97, 257–258 (2009)") has withstood the test of independent replication under truly blinded experimental conditions. No effect has therefore been widely accepted as scientifically proven[1](/articles/nature13290#ref-CR1 "International Commission for Non-Ionizing Radiation Protection. ICNIRP guidelines for limiting exposure to time-varying electric, magnetic, and electromagnetic fields (up to 300 GHz). Health Phys. 74, 494–522 (1998)"),[2](/articles/nature13290#ref-CR2 "International Commission for Non-Ionizing Radiation Protection. ICNIRP statement on the “Guidelines for limiting exposure to time-varying electric, magnetic, and electromagnetic fields (up to 300 GHz)”. Health Phys. 97, 257–258 (2009)"),[3](/articles/nature13290#ref-CR3 "World Health Organization. Extremely Low Frequency Fields. Environmental Health Criteria Monograph no. 238,. 
              http://www.who.int/peh-emf/publications/elf_ehc/en/
              
             (2007)"),[4](/articles/nature13290#ref-CR4 "Health Protection Agency. Health Effects from Radiofrequency Electromagnetic Fields. 
              http://www.hpa.org.uk/webc/HPAwebFile/HPAweb_C/1317133827077
              
             (2012)"),[5](/articles/nature13290#ref-CR5 "The INTERPHONE Study Group Brain tumour risk in relation to mobile telephone use: results of the INTERPHONE international case–control study. Int. J. Epidemiol. 39, 675–694 (2010)"),[6](/articles/nature13290#ref-CR6 "Johansen, C. et al. Cellular telephones and cancer—a nationwide cohort study in Denmark. J. Natl. Cancer Inst. 93, 203–207 (2001)"). 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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Acknowledgements

We thank M. Wuschek, Rohde & Schwarz, Bundesnetzagentur, and ETS Lindgren for help with measuring the electromagnetic fields, the workshops at the University of Oldenburg, especially T. Geiger, for building equipment, etc, and a large number of Bachelors, Masters and PhD students for help in conducting the experiments. We are grateful to the following for financial support: Defense Advanced Research Projects Agency (QuBE: N66001-10-1-4061 to P.J.H. and H.M.), VW-Stiftung (Lichtenberg professorship to H.M.), DFG (FOR 701 and MO 1408/2-2 to H.M.), Heinz Neumüller Stiftung (to C.M.H. and S.E.), BMBF (to H.M.), the European Research Council (to P.J.H.) and the EMF Biological Research Trust (to P.J.H.).

Author information

Author notes

  1. Svenja Engels and Nils-Lasse Schneider: These authors contributed equally to this work.

Authors and Affiliations

  1. Institut für Biologie und Umweltwissenschaften, Universität Oldenburg, D-26111 Oldenburg, Germany,
    Svenja Engels, Nils-Lasse Schneider, Nele Lefeldt, Christine Maira Hein, Manuela Zapka, Andreas Michalik, Dana Elbers & Henrik Mouritsen
  2. Research Centre for Neurosensory Sciences, University of Oldenburg, D-26111 Oldenburg, Germany,
    Svenja Engels, Nils-Lasse Schneider, Nele Lefeldt, Christine Maira Hein, Manuela Zapka, Andreas Michalik, Dana Elbers & Henrik Mouritsen
  3. Institute of Physics, University of Oldenburg, D-26111 Oldenburg, Germany,
    Achim Kittel
  4. Department of Chemistry, University of Oxford, Physical and Theoretical Chemistry Laboratory, Oxford OX1 3QZ, UK,
    P. J. Hore

Authors

  1. Svenja Engels
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  2. Nils-Lasse Schneider
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  3. Nele Lefeldt
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  4. Christine Maira Hein
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  5. Manuela Zapka
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  6. Andreas Michalik
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  7. Dana Elbers
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  8. Achim Kittel
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  9. P. J. Hore
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  10. Henrik Mouritsen
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Contributions

S.E. and N.-L.S. contributed equally to this work and are listed alphabetically. H.M. and N.-L.S. designed the study. S.E., N.L., C.M.H., M.Z., A.M. and D.E. performed the experiments. S.E., N.L., C.M.H., M.Z. and H.M. analysed the data. A.K., P.J.H. and N.-L.S. provided physical insight needed to properly produce and measure the electromagnetic fields. N.-L.S. and S.E. were in charge of generating the electromagnetic noise. N.-L.S. measured the electromagnetic fields. H.M., P.J.H., N.-L.S. and S.E. wrote most of the paper. All authors read and commented on the manuscript.

Corresponding author

Correspondence toHenrik Mouritsen.

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Extended data figures and tables

Extended Data Figure 1 Wooden huts and experimental locations.

a, Photograph of one of the four identical wooden huts used for our experiments. b, Photograph from the inside of an experimental hut showing the aluminium screening, parts of the Merritt coil system, and the table on which the funnels were placed. The insert shows the self-cutting screws used to connect the aluminium plates. c, Simple map of the city of Oldenburg. Built-up areas are shown in grey and nature-protected areas in green. Black lines denote highways, blue denotes water. Red stars: ‘1’ indicates the location of the University campus and ‘2’ the rural location used for some of the tests. d, Map of the University of Oldenburg Wechloy Campus. 1, main University building housing the biology, chemistry, physics and mathematics institutes; 2, botanical greenhouse; 3, iron-free wooden building; 4, the locations of the four wooden huts used for our experiments; 5, ‘Next Energy’ building.

Extended Data Figure 2 Electromagnetic noise measurements in the range from 40 Hz to 32 kHz.

a, Magnetic field intensity (B). b, Electric field intensity (E). The colour coding of the traces corresponds to Fig. 4. Notice that the frequency-axis (f) is logarithmic.

Extended Data Table 1 The accumulated time-dependent magnetic field intensity summed over all the frequencies in the spectra recorded for each behavioural test condition

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Engels, S., Schneider, NL., Lefeldt, N. et al. Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird.Nature 509, 353–356 (2014). https://doi.org/10.1038/nature13290

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Editorial Summary

Electromagnetic noise disrupts avian magnetic compass

Many migrating birds rely on the Earth's magnetic field for their sense of direction, although what mechanism they use to detect this extraordinarily weak field is unknown. Following the surprise observation that night-migratory songbirds (European robins) tested between autumn 2004 and autumn 2006 in wooden huts on the University of Oldenburg campus seemed unable to orient in the appropriate migratory direction, Henrik Mouritsen and colleagues performed controlled experiments to establish what was happening. They find that robins lose the ability to use the Earth's magnetic field when exposed to low-level AM electromagnetic noise between around 20 kz and 20 MHz, the kind of noise routinely generated by consumer electrical and electronic equipment. Interestingly, the magnetic component of this electromagnetic noise is a thousand times weaker than the lower exposure limits adopted in current World Health Organization (WHO) guidelines, yet it can disrupt the function of an entire sensory system in a higher vertebrate. The birds regain the ability to orient to the Earth's magnetic field when they are shielded from electromagnetic noise in the frequency range from 2 kHz to 5 MHz or when tested in a rural setting.

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