Broadband 75\u201385\xa0MHz radiofrequency fields disrupt magnetic compass orientation in night-migratory songbirds consistent with a flavin-based radical pair magnetoreceptor

Bo Leberecht,P J Hore,Siu Ying Wong,Michael Winklhofer,Shambhavi Apte,Raisa Chetverikova,Thiemo Karwinkel,Sara Döge,Glen Dautaj,Lars Burnus,Katrin Haase,Dmitry Kobylkov,Marco Bassetto,Henrik Mouritsen,Isabelle Musielak

doi:10.1007/s00359-021-01537-8

Abstract

The light-dependent magnetic compass sense of night-migratory songbirds can be disrupted by weak radiofrequency fields. This finding supports a quantum mechanical, radical-pair-based mechanism of magnetoreception as observed for isolated cryptochrome 4, a protein found in birds’ retinas. The exact identity of the magnetically sensitive radicals in cryptochrome is uncertain in vivo, but their formation seems to require a bound flavin adenine dinucleotide chromophore and a chain of four tryptophan residues within the protein. Resulting from the hyperfine interactions of nuclear spins with the unpaired electrons, the sensitivity of the radicals to radiofrequency magnetic fields depends strongly on the number of magnetic nuclei (hydrogen and nitrogen atoms) they contain. Quantum-chemical calculations suggested that electromagnetic noise in the frequency range 75–85 MHz could give information about the identity of the radicals involved. Here, we show that broadband 75–85 MHz radiofrequency fields prevent a night-migratory songbird from using its magnetic compass in behavioural experiments. These results indicate that at least one of the components of the radical pair involved in the sensory process of avian magnetoreception must contain a substantial number of strong hyperfine interactions as would be the case if a flavin–tryptophan radical pair were the magnetic sensor.

Highlights

Any putative magnetite-based sensor should not be affected by RF fields of the low intensity and frequency range used in the behavioural experiments (Kirschvink 1996; Ritz et al 2000)
We found that broadband RF fields are more effective at disrupting orientation performance compared to single-frequency RF fields, which conflicts with predictions for flavin adenine dinucleotide (FAD)·−-Z· (Ritz et al 2004; Engels et al 2014; Schwarze et al 2016)
In the normal geomagnetic field of Oldenburg (NMF), the group orientation of the birds that had not been exposed to 75–85 MHz RF fields resembled the north-easterly spring

Summary

Introduction

The magnetic compass of night-migratory songbirds (Wiltschko 1968) is an inclination compass (Wiltschko and Wiltschko 1972) that is light dependent (Wiltschko et al 1993; Zapka et al 2009; Mouritsen 2018) and involves the birds’ visual system (Mouritsen et al 2005, 2016; Heyers et al 2007; Zapka et al 2009, 2010). Most evidence suggests that the sensory mechanism is based on a radical pair process (Schulten et al 1978; Ritz et al 2000; Hore and Mouritsen 2016; Xu et al 2021), but the primary magnetic sensors have yet to be unequivocally identified. Very weak broadband radiofrequency (RF) fields from ~ 100 kHz to ~ 10 MHz prevent the birds from using their magnetic compass (Ritz et al 2004; Engels et al 2014; Schwarze et al 2016; Kobylkov et al 2019). A radical-pair-based mechanism seems to be consistent with a light-dependent magnetic sensor susceptible to weak RF fields at low MHz frequencies (Solovyov et al 2014; Hore and Mouritsen 2016)

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Conclusion