Magnetic compass of garden warblers is not affected by oscillating magnetic fields applied to their eyes

Abstract

The magnetic compass is an important element of the avian navigation system, which allows migratory birds to solve complex tasks of moving between distant breeding and wintering locations. The photochemical magnetoreception in the eye is believed to be the primary biophysical mechanism behind the magnetic sense of birds. It was shown previously that birds were disoriented in presence of weak oscillating magnetic fields (OMF) with frequencies in the megahertz range. The OMF effect was considered to be a fingerprint of the photochemical magnetoreception in the eye. In this work, we used miniaturized portable magnetic coils attached to the bird's head to specifically target the compass receptor. We performed behavioural experiments on orientation of long-distance migrants, garden warblers (Sylvia borin), in round arenas. The OMF with the amplitude of about 5 nT was applied locally to the birds' eyes. Surprisingly, the birds were not disoriented and showed the seasonally appropriate migratory direction. On the contrary, the same birds placed in a homogeneous 5 nT OMF generated by large stationary coils showed clear disorientation. On the basis of these findings, we suggest that the disruption of magnetic orientation of birds by oscillating magnetic fields is not related to photochemical magnetoreceptors in their eyes.

Figure 1

A garden warbler with attached portable device for local application of oscillating magnetic fields. Inset: The scheme of application of the oscillating magnetic field (OMF) to the head of a garden warbler. Blue and red dashed contours show, respectively, the boundaries of 2.5 nT and 5 nT OMF amplitude. Yellow circumference schematically shows the eyeball projection on the picture plane.

Figure 2

Orientation of garden warblers: (A) in the natural geomagnetic field (NMF); (B) in NMF plus homogenous 5 nT OMF generated by stationary coils at the frequency of 1.403 MHz; (C) in NMF with the portable device switched off; (D) in NMF with the portable OMF device switched on with local application of OMF to the bird’s eyes (as shown in the inset to Fig. 1). Dots show mean directions of individual birds in each experimental condition. Arrows show the second-order mean of the group of birds in each condition. The inner and outer dashed circles indicate 5 and 1% significance level of the Rayleigh test, respectively. Radial lines indicate 95% CI. The red triangle and letters mN are the position of the magnetic north.