Weak Broadband Electromagnetic Fields are More Disruptive to Magnetic Compass Orientation in a Night-Migratory Songbird (Erithacus rubecula) than Strong Narrow-Band Fields - PubMed (original) (raw)

Weak Broadband Electromagnetic Fields are More Disruptive to Magnetic Compass Orientation in a Night-Migratory Songbird (Erithacus rubecula) than Strong Narrow-Band Fields

Susanne Schwarze et al. Front Behav Neurosci. 2016.

Abstract

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.

Keywords: bird orientation; magnetic compass; magnetoreception; narrow-band electromagnetic field; radical pair mechanism; time-dependent electromagnetic fields.

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Figures

Figure 1

Figure 1

Ground plan of the new wooden laboratory. The materials used to build the laboratory were strictly non-magnetic. Four experimental chambers, which very efficiently screen time-dependent electromagnetic fields, are placed within the building. One double-wrapped, three-dimensional Merritt four-coil system with average coil diameters of ~2 m (Zapka et al., ; Hein et al., ; Engels et al., 2014) and a pair of 2.2 m _z_-axis RF-coils in Helmholtz-configuration was placed within three of these four chambers. (A) Cross-section. (B) Floor plan. (C) Photo of the new wooden laboratory from the outside. (D) Photo of one of the coil setups placed inside each of the three chambers. The photo also shows the nine Emlen funnels in their holders, which were placed on top of the wooden table in the center of the coil system.

Figure 2

Figure 2

Shielding effectiveness measurements in experimental chambers at different frequencies in accordance to the IEEE-299 standard (IEEE, 1997). *indicates that the shielding effectiveness was higher than the largest measurable value of 120 dB.

Figure 3

Figure 3

Magnetic and electric field measurements of test conditions in spring 2012, autumn 2013 and spring 2014. Traces in (A,B) show, respectively, the magnetic (B) and electric (E) components of the narrow-band electromagnetic fields and the artificial broadband noise as a function of frequency (f). The narrow-band magnetic fields had a peak intensity of 48 nT. The intensity of the broadband noise is shown twice: the purple line is the average (root mean square) intensity and the yellow line is the 40 min max-hold intensity and is directly comparable to the spectra shown in Engels et al. (2014).

Figure 4

Figure 4

Magnetic and electric field measurements of test conditions in spring 2013. Traces in (A–D) show, respectively, the magnetic (B) and electric (E) component of the narrow-band electromagnetic fields in the range from 10 kHz to 5 MHz (A,B) and in the range from 40 Hz to 32 kHz (C,D). The peak intensity in each condition was ~400 nT.

Figure 5

Figure 5

European robins can orient in their appropriate migratory directions when they are exposed to narrow-band time-dependent magnetic fields. (A–F): The results of orientation cage experiments on European robins. (A) Dummy condition in which the birds were not exposed to time-dependent magnetic fields (spring 2012, mean direction 17° ± 30° (95% confidence interval), r = 0.43, p < 0.01, N = 31). (B) Birds exposed to 1.363 MHz with a peak intensity of 48 nT (spring 2012, mean direction 358°, r = 0.25, p = 0.138, N = 31). (C) Birds exposed to 2.726 MHz with a peak intensity of 48 nT (spring 2012, mean direction 356°, r = 0.24, p = 0.179, N = 30). (D) Birds exposed to 50 Hz with a peak intensity of ~400 nT (spring 2013, 46° ± 50°, r = 0.45, p < 0.05, N = 19). (E) Birds exposed to 1.363 MHz with a peak intensity of ~400 nT (spring 2013, 38° ± 37°, r = 0.48, p < 0.01, N = 20). (F) Birds exposed to 2.726 MHz with a peak intensity of ~400 nT (spring 2013, 23° ± 35°, r = 0.49, p < 0.01, N = 20). Each dot represents the mean heading of an individual bird, the arrows indicate the group mean vector, the radial lines flanking the group mean vector indicate the 95% confidence interval for the group mean direction and the dashed circles represent the significance levels (p < 0.05 and p < 0.01) according to the Rayleigh test. mN, magnetic North.

Figure 6

Figure 6

Broadband electromagnetic noise disrupts the birds’ magnetic orientation capabilities whereas a narrow-band field at 1.315 MHz does not. The birds were able to orient in the dummy condition in the natural geomagnetic field (NMF), (A), mean direction 313° ± 34°, r = 0.54, p < 0.01, N = 16 and the changed magnetic field (CMF), (D), mean direction 96° ± 44°, r = 0.49, p < 0.05, N = 16 and when exposed to 1.315 MHz (NMF, (B), mean direction 281° ± 34°, r = 0.56, p < 0.01, N = 16; CMF, (E), 1.315 MHz: mean direction 20° ± 25°, r = 0.62, p < 0.001, N = 16). In contrast, the same birds were disoriented when exposed to artificial broadband noise (~2 kHz to ~9 MHz), NMF: (C), mean direction 265°, r = 0.17, p = 0.603, N = 16; CMF: (F), 21°, r = 0.19, p = 0.557, N = 16. All experiments were done in autumn 2013. For a description of the circular diagrams, see the legend to Figure 5. gN, geographic North.

Figure 7

Figure 7

Replication of the experiments from autumn 2013. (A,C) The birds’ orientation under the dummy condition in spring 2014. (B,D) The orientation of the birds during exposure to 1.315 MHz in spring 2014. The data in (A,B) were collected in an unchanged magnetic field (NMF, dummy: mean direction 89° ± 41°, r = 0.44, p < 0.05, N = 16; 1.315 MHz: mean direction 61° ± 26°, r = 0.64, p < 0.001, N = 18). The data in (C,D) were collected in a magnetic field turned 120° counterclockwise (CMF, dummy: mean direction 268° ± 46°, r = 0.42, p < 0.05, N = 18; 1.315 MHz: mean direction 218° ± 48°, r = 0.42, p < 0.05, N = 20). For a description of the circular diagrams, see the legend to Figure 5.

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