Abstract
One of the most unusual features of the avian magnetic compass is its sensitivity to weak oscillating magnetic fields (OMF) in the radiofrequency range. This effect, observed earlier in numerous experiments in European robins Erithacus rubecula and garden warblers Sylvia borin, is usually associated with the radical-pair magnetoreception in the eye, which is the mainstream biophysical model of the avian magnetic compass. We studied the effect of OMF on the orientation behavior of a long-distance migrant, the pied flycatcher Ficedula hypoleuca. The OMF with an amplitude of 190 nT disoriented pied flycatchers, similarly to the species studied earlier. However, the application of OMP with an amplitude of 17 nT did not lead to disorientation in pied flycatchers when tested in round arenas: the birds showed their correct season-specific migratory direction. This finding is in stark contrast with previous results, obtained in garden warblers at exactly the same place and under the same conditions: garden warblers were disoriented by OMF which was an order of magnitude weaker. Moreover, the threshold of sensitivity to OMF amplitude in pied flycatchers is found to be higher than that in both species previously studied, the European robin and the garden warbler. We discuss the variable sensitivity of avian compass to OMF in the context of migration ecology of two long-distance African migrants, the pied flycatcher and garden warbler, and the short-distance migrant, the European robin.
Significance statement
Birds are known to use a magnetic compass to determine the proper direction of their flight during seasonal migrations. Many previous experiments demonstrated that operation of this compass is disrupted by weak oscillating magnetic fields (OMF) in the radiofrequency range. Among the two bird species studied so far, a long-distance migrant, garden warbler, is more sensitive to OMF than a short-distance migrant, European robin. This might be a result of finer tuning of the magnetic compass of long-distance migrants, making it less robust to perturbations. In our experiments, however, the magnetic compass of another long-distance migrant, pied flycatcher, remained operational under OMF even stronger than that which disrupted magnetic orientation of European robins. This unexpected result demonstrates high variability of navigational systems of birds and raises questions about their adaptation to behavioral patterns of birds on their migration routes.
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Acknowledgements
We are grateful to Nadezda Romanova and Anisia Prokshina for assistance in the experiments. The authors acknowledge support from the Russian Science Foundation (grant 21-14-00158). We cordially thank Prof. Wolfgang Wiltschko and two anonymous reviewers for their helpful comments on an earlier version of the manuscript.
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JB, KK and NC conceived the research; RC developed the RF system; RC, KK, DS and AP installed the equipment and provided technical support for experiments, JB, KK, DS, AF and AP performed orientation tests and analysed the data; JB, KK, AP and NC wrote the paper. All authors commented on the manuscript. All authors gave final approval for publication and agree to be held accountable for the work performed therein.
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All animal procedures (in this case, capture of the birds and simple, non-invasive, behavioural experiments) were approved by the appropriate authorities: Permit 24/2018–06 by Kaliningrad Regional Agency for Protection, Reproduction and Use of Animal World and Forests; and Permit 6–2021 by the Bioethics Committee of Sechenov Institute of Evolutionary Physiology and Biochemistry RAS. All experiments were performed in accordance with relevant guidelines and regulations. The birds were released back into the wild after all experiments had been completed.
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Bojarinova, J., Kavokin, K., Cherbunin, R. et al. Sensitivity threshold of avian magnetic compass to oscillating magnetic field is species-specific. Behav Ecol Sociobiol 77, 6 (2023). https://doi.org/10.1007/s00265-022-03282-7
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DOI: https://doi.org/10.1007/s00265-022-03282-7