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A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons

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Abstract

Animals make use of the Earth’s magnetic field for navigation and regulation of vegetative functions; however, the anatomical and physiological basis for the magnetic sense has not been elucidated yet. Our recent results from histology and X-ray analyses support the hypothesis that delicate iron-containing structures in the skin of the upper beak of homing pigeons might serve as a biological magnetometer. Histology has revealed various iron sites within dendrites of the trigeminal nerve, their arrangement along strands of axons, the existence of three dendritic fields in each side of the beak with specific 3D-orientations, and the bilateral symmetry of the whole system. Element mapping by micro-synchrotron X-ray fluorescence analysis has shown the distribution of iron and its quantities. Micro-synchrotron X-ray absorption near-edge-structure spectroscopy has allowed us to unambiguously identify maghemite as the predominating iron mineral (90 vs 10% magnetite). In this paper, we show that iron-based magnetoreception needs the presence of both of these iron minerals, their specific dimensions, shapes, and arrangements in three different subcellular compartments. We suggest that an inherent magnetic enhancement process via an iron-crusted vesicle and the attached chains of iron platelets might be sufficient to account for the sensitivity and specificity required by such a magnetoreceptor. The appropriate alignment between the Earth’s magnetic field and the maghemite bands would induce a multiple attraction of the magnetite bullets perpendicular to the membrane, thus, triggering strain-sensitive membrane channels and a primary receptor potential. Due to its 3D architecture and physicochemical nature, the dendritic system should be able to separately sense the three vector components of the Earth’s local field, simultaneously—allowing birds to detect their geographic position by the magnetic vector, i.e., amplitude and direction of the local magnetic field, irrespective of the animal’s posture or movement and photoreception.

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Acknowledgments

W. and R. Wiltschko (University Frankfurt a. M.) and P. Schlegel (University Munich) gave helpful comments on data presented in this paper and discussed the theories supporting our model. P. Brownell (University Corvallis, Oregon) critically commented on the receptor physiological part of the model. We acknowledge the support by M. Wilke (University Potsdam) during the μ-XANES experiments and C. Taylor-Dorenkamp (University Boston) who helped us improve the English version of the text. We also thank the reviewers of an earlier version of the manuscript who gave helpful and encouraging comments. We thank E. Thielen, M. Stöhr (both at University Frankfurt a. M.) and W. Hofer (MPI Hirnforschung, Frankfurt a. M.) for their expert technical help in the histology labs. This project is supported by grants from the Deutsche Forschungsgemeinschaft to G. F. (Fl 177/15-1) and HASYLAB at DESY Hamburg to B.S. (I-04-012, I-05-095). All experimental procedures followed the legal requirements of the German law for the protection of animals.

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  1. AG NCR, FB Biowissenschaften, J. W. Goethe-Universität, Siesmayerstr. 70, D-60054, Frankfurt a. M., Germany

    Gerta Fleissner, Branko Stahl, Peter Thalau & Günther Fleissner

  2. Hamburger Synchrotronstrahlungslabor HASYLAB, Deutsches Elektronen-Synchrotron DESY, Notkestr 85, D-22603, Hamburg, Germany

    Gerald Falkenberg

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  1. Gerta Fleissner
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  2. Branko Stahl
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Correspondence to Gerta Fleissner.

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Fleissner, G., Stahl, B., Thalau, P. et al. A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons. Naturwissenschaften 94, 631–642 (2007). https://doi.org/10.1007/s00114-007-0236-0

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