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.

Magnetic compass orientation in night-migratory songbirds is embedded in the visual system and seems to be based on a light-dependent radical pair mechanism. Recent findings suggest that both broadband electromagnetic fields ranging from ~2 kHz to ~9 MHz and narrow-band fields at the so-called Larmor frequency for a free electron in the Earth’s magnetic field can disrupt this mechanism. However, due to local magnetic fields generated by nuclear spins, effects specific to the Larmor frequency are difficult to understand considering that the primary sensory molecule should be organic and probably a protein. We therefore constructed a purpose-built laboratory and tested the orientation capabilities of European robins in an electromagnetically silent environment, under the specific influence of four different oscillating narrow-band electromagnetic fields, at the Larmor frequency, double the Larmor frequency, 1.315 MHz or 50 Hz, and in the presence of broadband electromagnetic noise covering the range from ~2 kHz to ~9 MHz. Our results indicated that the magnetic compass orientation of European robins could not be disrupted by any of the relatively strong narrow-band electromagnetic fields employed here, but that the weak broadband field very efficiently disrupted their orientation.

Migratory birds are known to use the Earth's magnetic field as an orientation cue on their tremendous journeys between their breeding and overwintering grounds. The magnetic compass of migratory birds relies on the magnetic field's inclination, i.e. the angle between the magnetic field lines and the Earth's surface. As a consequence, vertical or horizontal field lines corresponding to 0 or 90 deg inclination should offer no utilizable information on where to find North or South. So far, very little is known about how small the deviations from horizontal or vertical inclination are that migratory birds can detect and use as a reference for their magnetic compass. Here, we asked: what is the steepest inclination angle at which a migratory bird, the Eurasian blackcap (Sylvia atricapilla), can still perform magnetic compass orientation in Emlen funnels? Our results show that blackcaps are able to orient in an Earth's strength magnetic field with inclination angles of 67 and 85 deg, but fail to orient in a field with 88 deg inclination. This suggests that the steepest inclination angle enabling magnetic compass orientation in migratory blackcaps tested in Emlen funnels lies between 85 and 88 deg. KEY WORDS: Bird navigation, Magnetic inclination compass, Functional range, Magnetoreception, Radical-pair mechanism, Sylvia atricapilla INTRODUCTIONFor 50 years, it has been known that birds are able to use the Earth's magnetic field for orientation (Merkel and Wiltschko, 1965). In contrast to a man-made compass that works on the basis of the polarity of the magnetic field, the bird's magnetic compass is an inclination compass (Wiltschko and Wiltschko, 1972;Wiltschko and Wiltschko, 1995). This means that birds do not differentiate between North and South but between poleward and equatorward (the direction in which the field lines and the Earth's surface form the smaller angle is defined as equatorward) (Wiltschko and Wiltschko, 1972;Wiltschko and Wiltschko, 1995). Therefore, at the magnetic equator or at the magnetic poles, where the inclination is 0 and 90 deg, respectively, the birds are faced with the problem that the Earth's magnetic field provides no or ambiguous directional information. In other words, there is no larger or smaller inclination angle to detect. Wiltschko and Wiltschko (Wiltschko and Wiltschko, 1992) suggested that for transequatorial migrants, the crossing of the equator serves as a trigger and changes the heading from equatorward to poleward. Cochran et al. (Cochran et al., 2004) suggested that the magnetic compass can be calibrated by celestial RESEARCH ARTICLEAG Neurosensorik/Animal Navigation, Institute of Biological and Environmental Sciences, University Oldenburg, D-26111 Oldenburg, Germany. *These authors contributed equally to this work ‡ Author for correspondence (nele.lefeldt@uni-oldenburg.de) Received 2 May 2014; Accepted 12 November 2014 cues and that this mechanism might help birds to cross the magnetic equator. Even with these suggestions, an interesting question remains: how wide...

Magnetoreception remains one of the few unsolved mysteries in sensory biology. The upper beak, which is innervated by the ophthalmic branch of the trigeminal nerve (V1), has been suggested to contain magnetic sensors based on ferromagnetic structures. Recently, its existence in pigeons has been seriously challenged by studies suggesting that the previously described iron-accumulations are macrophages, not magnetosensitive nerve endings. This raised the fundamental question of whether V1 is involved in magnetoreception in pigeons at all. We exposed pigeons to either a constantly changing magnetic field (CMF), to a zero magnetic field providing no magnetic information, or to CMF conditions after V1 was cut bilaterally. Using immediate early genes as a marker of neuronal responsiveness, we report that the trigeminal brainstem nuclei of pigeons, which receive V1 input, are activated under CMF conditions and that this neuronal activation disappears if the magnetic stimuli are removed or if V1 is cut. Our data suggest that the trigeminal system in pigeons is involved in processing magnetic field information and that V1 transmits this information from currently unknown, V1-associated magnetosensors to the brain.

Previous studies on European robins, Erithacus rubecula, and Australian silvereyes, Zosterops lateralis, had suggested that magnetic compass information is being processed only in the right eye and left brain hemisphere of migratory birds. However, recently it was demonstrated that both garden warblers, Sylvia borin, and European robins have a magnetic compass in both eyes. These results raise the question if the strong lateralization effect observed in earlier experiments might have arisen from artifacts or from differences in experimental conditions rather than reflecting a true all-or-none lateralization of the magnetic compass in European robins. Here we show that (1) European robins having only their left eye open can orient in their seasonally appropriate direction both during autumn and spring, i.e. there are no strong lateralization differences between the outward journey and the way home, that (2) their directional choices are based on the standard inclination compass as they are turned 180° when the inclination is reversed, and that (3) the capability to use the magnetic compass does not depend on monocular learning or intraocular transfer as it is already present in the first tests of the birds with only one eye open.