Testing for the presence of magnetite in the upper-beak skin of homing pigeons (original) (raw)

Abstract

We carried out magnetic and nonmagnetic experiments on fresh, upper-beak skin tissue samples isolated from six pairs of homing pigeons to test whether the tissue contains magnetite particles. Results of (1) room-temperature isothermal remanent magnetization (IRM) acquisition and alternating field (AF) demagnetization, (2) low-temperature demagnetization of saturation IRM acquired at 5 K in a field of 5 tesla (T) (SIRM5 K) after zero-field cooled (ZFC) and field cooled (FC) treatments, and (3) cycling of the saturation IRM acquired at 300 K in a field of 5 T (SIRM300 K) between 5 and 300 K, indicate the presence of magnetite in the measured samples. A significant loss of SIRM5 K below 20 K suggests the dominance of superparamagnetic (SPM) particles. The SIRM acquisition capacity of the female pigeon is stronger than that of the male pigeon in all four measured pairs, suggesting for the first time that the magnetite concentration is probably sex dependent. Light microscopic observation on the histological sections stained with Prussian Blue detected the presence of some tiny, dotted, dark-blue staining Fe3+ aggregates (size 1–4 µm) located directly beneath the subcutis within strands of connective tissue, nearby the rim of the regions full of red nuclei. The results of this study support the idea that homing pigeons may have a magnetite-based receptor, which potentially could be used for sensing the Earth’s magnetic field during navigation.

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References

• Bunting H (1949) The histochemical detection of iron in tissue. Stain Technol 24:109–115
  CAS Google Scholar
• Davila AF, Fleissner G, Winklhofer M, Petersen N (2003) A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite. Phys Chem Earth 28:647–652
  Google Scholar
• Dunlop DJ, Özdemir Ö (1997) Rock magnetism: fundamentals and frontiers. Cambridge, Cambridge University Press. 573 pp
  Google Scholar
• Fleissner G, Holtkamp-Rötzler E, Hanzlik M et al (2003) Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J Comp Neurol 458:350–360
  Article PubMed CAS Google Scholar
• 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 13:325–331
  Article PubMed CAS Google Scholar
• Keeton WT, Larkin TS, Windson DM (1974) Normal fluctuation in the earth’s magnetic field influence pigeon orientation. J Comp Physiol 95:95–103
  Article Google Scholar
• Mora CV, Davison M, Wild JM, Walker MM (2004) Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432:508–511
  Article PubMed CAS Google Scholar
• Moskowitz BM, Frankel RB, Bazylinski DA (1993) Rock magnetic criteria for the detection of biogenic magnetite. Earth Planet Sci Lett 120:283–300
  Article Google Scholar
• Pan YX, Petersen N, Winklhofer M et al (2005) Rock magnetic properties of uncultured magnetotactic bacteria. Earth Planet Sci Lett 237:311–325
  Article CAS Google Scholar
• Presti D, Pettigrew JD (1980) Ferromagnetic coupling to muscle receptors as a basis for geomagnetic field sensitivity in animals. Nature 285:99–101
  Article PubMed CAS Google Scholar
• Romeis B (1968) Miikroskopische Technik. Munich, Oldenbourg-Verlag. 183 pp
  Google Scholar
• Semm P, Nohr D, Demaine C, Wiltschko W (1984) Neural basis of the magnetic compass: interactions of visual, magnetic and vestibular inputs in the pigeon’s brain. J Comp Physiol A155:283–288
  Article Google Scholar
• Semm P, Demaine C (1986) Neurophysiological properties of magnetic cells in the visual system of the pigeon. J Comp Physiol 159:619–625
  Article CAS Google Scholar
• Verwey EJW (1939) Electronic conduction of magnetite (Fe3O4) and its transition point at low-temperature. Nature 44:327–328
  Google Scholar
• Walcott C, Green RP (1974) Orientation of homing pigeons altered by a change in the direction of an applied magnetic field. Science 184:180–182
  Article PubMed CAS Google Scholar
• Walcott C, Gould JL, Kirschvink JL (1979) Pigeons have magnets. Science 205:1027–1029
  Article PubMed CAS Google Scholar
• Wang ZN, An N (2004) Encyclopaedia of pigeon cultivation (homing pigeon, ornamental pigeon and meat pigeon). Beijing, China Agriculture Press (in Chinese)
  Google Scholar
• Williams MN, Wild JM (2001) Trigeminally innervated iron containing structures in the beak of homing pigeons, and other birds. Brain Res 889:243–246
  Article PubMed CAS Google Scholar
• Wiltschko R, Wiltschko W (1995) Magnetic orientation of animals. Berlin, Springer-Verlag
  Google Scholar
• Winklhofer M, Holtkamp-Rötzler E, Hanzlik M, Fleissner G, Petersen N (2001) Clusters of superparamagnetic magnetic particles in the upper-beak skin of homing pigeons: evidence of a magnetoreceptor? Eur J Mineral 13:659–669
  Article CAS Google Scholar

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Acknowledgements

We thank Professor Mi Ma at the Institute of Botany (CAS) for kind permission for the use of microtomes. The authors gratefully acknowledge the anonymous reviewers for very careful review and very constructive comments, Professor Nikolai Petersen for useful suggestions, and Dr. Mimi Hill for improving the English of this manuscript. This work was financially supported by the grants of the Chinese Academy of Sciences (KZCX-3-SW-150) and the National Science Foundation of China (40221402 and 40325011).

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Authors and Affiliations

1. Paleomagnetism and Geochronology Laboratory (SKL-LE), Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing, 100029, China
   Lanxiang Tian, Bo Xiao, Wei Lin, Rixiang Zhu & Yongxin Pan
2. Institute of Zoology, Chinese Academy of Sciences, Beijing, 100080, China
   Shuyi Zhang

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1. Lanxiang Tian
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2. Bo Xiao
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3. Wei Lin
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4. Shuyi Zhang
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5. Rixiang Zhu
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6. Yongxin Pan
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Correspondence toYongxin Pan.

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Tian, L., Xiao, B., Lin, W. et al. Testing for the presence of magnetite in the upper-beak skin of homing pigeons.Biometals 20, 197–203 (2007). https://doi.org/10.1007/s10534-006-9027-x

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• Received: 28 March 2006
• Accepted: 20 June 2006
• Published: 10 August 2006
• Issue Date: April 2007
• DOI: https://doi.org/10.1007/s10534-006-9027-x

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