, Volume 94, Issue 8, pp 631–642 | Cite as

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

  • Gerta FleissnerEmail author
  • Branko Stahl
  • Peter Thalau
  • Gerald Falkenberg
  • Günther Fleissner
Original Paper


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.


Biological magnetometer Maghemite Magnetite XRFS XANES 



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.


  1. Abracado LG, Esquivel DM, Alves OC, Wajnberg E (2005) Magnetic material in head, thorax, and abdomen of Solenopsis substituta ants: a ferromagnetic resonance study. J Magn Reson 175:309–316PubMedCrossRefGoogle Scholar
  2. Arcas J, Hernando A, Barandiaran JM, Prados C, Vazquez M, Marin P, Neuweiler A (1998) Soft to hard magnetic anisotropy in nanostructured magnets. Phys Rev B 58:5193–5196CrossRefGoogle Scholar
  3. Bacri JC, Salin D, Massart R (1982) Study of the deformation of ferrofluid droplets in a magnetic field. J Physique Lett 43:L179–L183CrossRefGoogle Scholar
  4. Bazylinski DA (1999) Synthesis of the bacterial magnetosome: the making of a magnetic personality. Int Microbiol 2:71–80PubMedGoogle Scholar
  5. Beason RC (2005) Mechanisms of magnetic orientation in birds. Integr Comp Biol 45:565–573CrossRefGoogle Scholar
  6. Beason RC, Semm P (1987) Magnetic responses of the trigeminal nerve system of the bobolink (Dolichonyx oryzivorus). Neurosci Lett 80:229–234PubMedCrossRefGoogle Scholar
  7. Beason RC, Semm P (1996) Does the avian ophthalmic nerve carry magnetic navigational information? J Exp Biol 199:1241–1244PubMedGoogle Scholar
  8. Becker M (2000) Die Nutzung des Erdmagnetfeldes innerhalb der Navigation von Brieftauben (Columba livia). PhD thesis, Universität Frankfurt a. MGoogle Scholar
  9. Davila A, Fleissner G, Winklhofer M, Petersen N (2003) A new model for a magnetoreceptor in homing pigeons based on interacting cluster s of superparamagnetic magnetite. Phys Chem Earth 28:647–652Google Scholar
  10. Diebel CE, Proksch R, Green CR, Neilson P, Walker MM (2000) Magnetite defines a vertebrate magnetoreceptor. Nature 406:299–302PubMedCrossRefGoogle Scholar
  11. Dubbeldam JL (1998) The sensory trigeminal system in birds: input, organization and effects of peripheral damage. A review. Arch Physiol Biochem 106:338–345PubMedCrossRefGoogle Scholar
  12. Fleissner G, Stahl B (2005) Magnetrezeption bei Brieftauben. In: Rossmann T, Tropea C (eds) Bionik. Springer, Berlin, pp 501–515CrossRefGoogle Scholar
  13. Fleissner G, Holtkamp-Rötzler E, Hanzlik M, Winklhofer M, Fleissner G, Petersen N, Wiltschko W (2003) Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J Comp Neurol 458:350–360PubMedCrossRefGoogle Scholar
  14. Fransson T, Jakobsson S, Johansson P, Kullberg C, Lind J, Vallin A (2001) Bird migration: magnetic cues trigger extensive refuelling. Nature 414:35–36PubMedCrossRefGoogle Scholar
  15. Hanzlik M, Heunemann C, Holtkamp-Rötzler E, Winklhofer M, Petersen N, Fleissner G (2000) Superparamagnetic magnetite in the upper beak tissue of homing pigeons. BioMetals 13:325–331PubMedCrossRefGoogle Scholar
  16. Herzer G (1997) Nanocrystalline soft magnetic alloys. In: Buschow KHJ (ed) Handbook of magnetic materials, vol 10. Elsevier, Amsterdam, pp 415–462Google Scholar
  17. Irwin WP, Lohmann KJ (2003) Magnet-induced disorientation in hatchling sea turtles. J Exp Biol 206:497–501PubMedCrossRefGoogle Scholar
  18. Irwin WP, Lohmann KJ (2005) Disruption of magnetic orientation in hatchling loggerhead sea turtles by pulsed magnetic fields. J Comp Physiol A 191:475–480CrossRefGoogle Scholar
  19. Janssens KHA, Adams FCV, Rindby A (2000) Microscopic X-ray fluorescence analysis. Wiley, ChichesterGoogle Scholar
  20. Johnsen S, Lohmann KJ (2005) The physics and neurobiology of magnetoreception. Nat Rev Neurosci 6:703–712PubMedCrossRefGoogle Scholar
  21. Kalmijn AJ (1978) Experimental evidence of geomagnetic orientation in elasmobranch fishes. In: Schmitt-Koenig K, Keeton WT (eds) Animal migration, navigation and homing. Springer, Berlin, Heidelberg New York, pp 347–353Google Scholar
  22. Keeton WT, Larkin TS, Windsor DM (1974) Normal fluctuations of the earth’s magnetic field influence pigeon orientation. J Comp Physiol 95:95–103CrossRefGoogle Scholar
  23. Kirschvink JL, Gould JL (1981) Biogenic magnetite as a basis for magnetite-based magnetic field detection in animals. Biosystems 13:181–201PubMedCrossRefGoogle Scholar
  24. Kirschvink JL, Hagadorn JW (2000) A grand unified theory of biomineralisation. In: Bäuerlein E (ed) The biomineralisation of nano- and microstructures. Wiley-VCH Verlag, Weinheim, pp 139–150Google Scholar
  25. Kirschvink JL, Walker MM, Diebel CE (2001) Magnetite-based magnetoreception. Curr Opin Neurobiol 11:462–467PubMedCrossRefGoogle Scholar
  26. Kung C (2005) A possible unifying principle for mechanosensation. Nature 436:647–654PubMedCrossRefGoogle Scholar
  27. Mann S, Sparks NH, Walker MM, Kirschvink JL (1988) Ultrastructure, morphology and organization of biogenic magnetite from sockeye salmon, Oncorhynchus nerka: implications for magnetoreception. J Exp Biol 140:35–49PubMedGoogle Scholar
  28. Marhold S, Burda H, Wiltschko W (1997) A magnetic polarity compass for direction finding in a subterranean mammal. Naturwissenschaften 84:421–423CrossRefGoogle Scholar
  29. Mora CV, Davison M, Wild JM, Walker MM (2004) Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432:508–511PubMedCrossRefGoogle Scholar
  30. Mouritsen H, Ritz T (2005) Magnetoreception and its use in bird navigation. Curr Opin Neurobiol 15:406–414PubMedCrossRefGoogle Scholar
  31. Nemec PJ, Altmann J, Marhold S, Burda H, Oelschläger HHA (2001) Neuroanatomy of magnetoreception: the superior colliculus involved in magnetic orientation in a mammal. Science 294:366–368PubMedCrossRefGoogle Scholar
  32. Phillips JB, Borland SC (1992) Behavioural evidence for use of a light-dependent magnetoreception mechanism by a vertebrate. Nature 359:142–144CrossRefGoogle Scholar
  33. Quintana C, Bellefqih S, Laval JY, Guerquin-Kern JL, Wu TD, Avila J, Ferrer I, Arranz R, Patino C (2006) Study of the localization of iron, ferritin, and hemosiderin in Alzheimer’s disease hippocampus by analytical microscopy at the subcellular level. J Struct Biol 153(1):42–54PubMedCrossRefGoogle Scholar
  34. Ritz T, Adem S, Schulten K (2000) A model for photoreceptor-based magnetoreception in birds. Biophys J 78:707–718PubMedCrossRefGoogle Scholar
  35. Schulten K (1982) Magnetic field effects in chemistry and biology. In: Treusch J (ed) Festkörperprobleme, vol 22. Vieweg, Braunschweig, pp 61–83Google Scholar
  36. Shcherbakov VP, Winklhofer M (1999) The osmotic magnetometer: a new model for a magnetite-based magnetoreceptor in animals. Eur Biophys J 28:380–392CrossRefGoogle Scholar
  37. Stahl B, Fleissner G, Barnert E, Falkenberg G (2006a) Element scanning by μXRF in putative magnetic field receptors in the upper beak skin of homing pigeons. HASYLAB Annual Report 2005. DESY, Hamburg, pp 1029–1030Google Scholar
  38. Stahl B, Fleissner G, Falkenberg G, Fleissner G (2006b) Magnetite nanoparticles alone are not able to explain iron mineral-based magnetoreception in homing pigeons. In: Kyriakopoulos A, Michalke B, Graebert A, Behne D (eds) Proceedings of the 4th fall conference on metalloproteins and metalloidproteins. Herbert Utz Verlag, München, pp 63–68Google Scholar
  39. Stahl B, Fleissner G, Fleissner G, Falkenberg G (2007a) Cross-species unveiling of a putative avian magnetoreceptor. HASYLAB Annual Report 2006. DESY, Hamburg, 1269–1270Google Scholar
  40. Stahl B, Fleissner G, Fleissner G, Holub-Krappe E (2007b) Micromagnetic aspects of magnetoreception of homing pigeons based on iron minerals. XAFS 13 Proceedings, American Inst Physics 882:755–757Google Scholar
  41. Walker M, Diebel CE, Haugh CV, Pankhurst PM, Montgomery JC, Green CR (1997) Structure and function of the vertebrate magnetic sense. Nature 390:371–376CrossRefGoogle Scholar
  42. Wang JH, Shaun SD, Cain D, Lohmann KJ (2003) Identification of magnetically responsive neurons in the marine mollusc Tritonia diomedea. J Exp Biol 206:381–388PubMedCrossRefGoogle Scholar
  43. Wilke M, Farges F, Petit PE, Brown GE Jr, Martin F (2001) Oxidation state and coordination of Fe in minerals: an Fe K XANES spectroscopic study. Am Mineral 86:714–730Google Scholar
  44. Wiltschko R, Wiltschko W (1995) Magnetic orientation in animals. Springer, Berlin, Heidelberg New YorkGoogle Scholar
  45. Wiltschko W, Wiltschko R (1997) Magnetic orientation in birds. J Exp Biol 199:29–38Google Scholar
  46. Wiltschko W, Munro U, Ford H, Wiltschko R (2003) Magnetic orientation in birds: non-compass responses under monochromatic light of increased intensity. Proc R Soc Lond B 270:2133–2140CrossRefGoogle Scholar
  47. Wiltschko W, Wiltschko R (2005) Magnetic orientation and magnetoreception in birds and other animals. J Comp Physiol A 191:675–693CrossRefGoogle Scholar
  48. Wiltschko W, Munro U, Wiltschko R, Kirschvink JL (2002) Magnetite-based magnetoreception in birds: the effect of a biasing field and a pulse on migratory behavior. J Exp Biol 205:3031–3037PubMedGoogle Scholar
  49. Winklhofer M, Holtkamp-Rötzler E, Hanzlik M, Fleissner G, Petersen N (2001) Clusters of superparamagnetic magnetite particles in the upper beak skin of homing pigeons: evidence of a magnetoreceptor? Eur J Mineral 13:659–669CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Gerta Fleissner
    • 1
    Email author
  • Branko Stahl
    • 1
  • Peter Thalau
    • 1
  • Gerald Falkenberg
    • 2
  • Günther Fleissner
    • 1
  1. 1.AG NCR, FB Biowissenschaften, J. W. Goethe-UniversitätFrankfurt a. M.Germany
  2. 2.Hamburger Synchrotronstrahlungslabor HASYLAB, Deutsches Elektronen-Synchrotron DESYHamburgGermany

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