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Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons

Nature volume 484, pages 367–370 (2012)Cite this article

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Abstract

Understanding the molecular and cellular mechanisms that mediate magnetosensation in vertebrates is a formidable scientific problem1,2. One hypothesis is that magnetic information is transduced into neuronal impulses by using a magnetite-based magnetoreceptor3,4. Previous studies claim to have identified a magnetic sense system in the pigeon, common to avian species, which consists of magnetite-containing trigeminal afferents located at six specific loci in the rostral subepidermis of the beak5,6,7,8. These studies have been widely accepted in the field and heavily relied upon by both behavioural biologists and physicists9,10,11. Here we show that clusters of iron-rich cells in the rostro-medial upper beak of the pigeon Columbia livia are macrophages, not magnetosensitive neurons. Our systematic characterization of the pigeon upper beak identified iron-rich cells in the stratum laxum of the subepidermis, the basal region of the respiratory epithelium and the apex of feather follicles. Using a three-dimensional blueprint of the pigeon beak created by magnetic resonance imaging and computed tomography, we mapped the location of iron-rich cells, revealing unexpected variation in their distribution and number—an observation that is inconsistent with a role in magnetic sensation. Ultrastructure analysis of these cells, which are not unique to the beak, showed that their subcellular architecture includes ferritin-like granules, siderosomes, haemosiderin and filopodia, characteristics of iron-rich macrophages. Our conclusion that these cells are macrophages and not magnetosensitive neurons is supported by immunohistological studies showing co-localization with the antigen-presenting molecule major histocompatibility complex class II. Our work necessitates a renewed search for the true magnetite-dependent magnetoreceptor in birds.

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Figure 1: PB-positive cells in the upper beak.
Figure 2: Number and distribution of PB-positive cells in the upper beak.
Figure 3: Ultrastructure of PB-positive cells.
Figure 4: MHC II immunohistochemistry on PB-positive cells.

References

  1. Mouritsen, H. & Ritz, T. Magnetoreception and its use in bird navigation. Curr. Opin. Neurobiol. 15, 406–414 (2005)

    Article  CAS  Google Scholar 

  2. Johnsen, S. & Lohmann, K. J. The physics and neurobiology of magnetoreception. Nature Rev. Neurosci. 6, 703–712 (2005)

    Article  CAS  Google Scholar 

  3. Mora, C. V., Davison, M., Wild, J. M. & Walker, M. M. Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432, 508–511 (2004)

    Article  ADS  CAS  Google Scholar 

  4. Kirschvink, J. L., Walker, M. M. & Diebel, C. E. Magnetite-based magnetoreception. Curr. Opin. Neurobiol. 11, 462–467 (2001)

    Article  CAS  Google Scholar 

  5. Fleissner, G. et al. Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 458, 350–360 (2003)

    Article  CAS  Google Scholar 

  6. Falkenberg, G. et al. Avian magnetoreception: elaborate iron mineral containing dendrites in the upper beak seem to be a common feature of birds. PLoS ONE 5, e9231 (2010)

    Article  ADS  Google Scholar 

  7. Fleissner, G., Stahl, B., Thalau, P., Falkenberg, G. & Fleissner, G. A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons. Naturwissenschaften 94, 631–642 (2007)

    Article  ADS  CAS  Google Scholar 

  8. Hanzlik, M. et al. Superparamagnetic magnetite in the upper beak tissue of homing pigeons. Biometals 13, 325–331 (2000)

    Article  CAS  Google Scholar 

  9. Wiltschko, R., Schiffner, I., Fuhrmann, P. & Wiltschko, W. The role of the magnetite-based receptors in the beak in pigeon homing. Curr. Biol. 20, 1534–1538 (2010)

    Article  CAS  Google Scholar 

  10. Solov’yov, I. A. & Greiner, W. Theoretical analysis of an iron mineral-based magnetoreceptor model in birds. Biophys. J. 93, 1493–1509 (2007)

    Article  ADS  Google Scholar 

  11. Davila, A. F., Winklhofer, M., Shcherbakov, V. P. & Petersen, N. Magnetic pulse affects a putative magnetoreceptor mechanism. Biophys. J. 89, 56–63 (2005)

    Article  CAS  Google Scholar 

  12. Zapka, M. et al. Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461, 1274–1277 (2009)

    Article  ADS  CAS  Google Scholar 

  13. Ritz, T., Thalau, P., Phillips, J. B., Wiltschko, R. & Wiltschko, W. Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429, 177–180 (2004)

    Article  ADS  CAS  Google Scholar 

  14. Cadiou, H. & McNaughton, P. A. Avian magnetite-based magnetoreception: a physiologist’s perspective. J. R. Soc. Interface 7 (suppl. 2). S193–S205 (2010)

    Article  CAS  Google Scholar 

  15. Beason, R. C. & Semm, P. Magnetic responses of the trigeminal nerve system of the bobolink (Dolichonyx oryzivorus). Neurosci. Lett. 80, 229–234 (1987)

    Article  CAS  Google Scholar 

  16. Heyers, D., Zapka, M., Hoffmeister, M., Wild, J. M. & Mouritsen, H. Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. Proc. Natl Acad. Sci. USA 107, 9394–9399 (2010)

    Article  ADS  CAS  Google Scholar 

  17. Williams, M. N. & Wild, J. M. Trigeminally innervated iron-containing structures in the beak of homing pigeons, and other birds. Brain Res. 889, 243–246 (2001)

    Article  CAS  Google Scholar 

  18. Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. Avian orientation: the pulse effect is mediated by the magnetite receptors in the upper beak. Proc. Biol. Sci. 276, 2227–2232 (2009)

    Article  Google Scholar 

  19. Solov’yov, I. A. & Greiner, W. Micromagnetic insight into a magnetoreceptor in birds: existence of magnetic field amplifiers in the beak. Phys. Rev. E 80, 041919 (2009)

    Article  ADS  Google Scholar 

  20. Stapput, K., Thalau, P., Wiltschko, R. & Wiltschko, W. Orientation of birds in total darkness. Curr. Biol. 18, 602–606 (2008)

    Article  CAS  Google Scholar 

  21. Iancu, T. C. Ferritin and hemosiderin in pathological tissues. Electron Microsc. Rev. 5, 209–229 (1992)

    Article  CAS  Google Scholar 

  22. Richter, G. W. The iron-loaded cell—the cytopathology of iron storage. A review. Am. J. Pathol. 91, 362–404 (1978)

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Wang, J. & Pantopoulos, K. Regulation of cellular iron metabolism. Biochem. J. 434, 365–381 (2011)

    Article  CAS  Google Scholar 

  24. Mebius, R. E. & Kraal, G. Structure and function of the spleen. Nature Rev. Immunol. 5, 606–616 (2005)

    Article  CAS  Google Scholar 

  25. Meguro, R. et al. The presence of ferric and ferrous iron in the nonheme iron store of resident macrophages in different tissues and organs: histochemical demonstrations by the perfusion-Perls and -Turnbull methods in the rat. Arch. Histol. Cytol. 68, 171–183 (2005)

    Article  CAS  Google Scholar 

  26. Simson, J. V. & Spicer, S. S. Ferritin particles in macrophages and in associated mast cells. J. Cell Biol. 52, 536–541 (1972)

    Article  CAS  Google Scholar 

  27. Igyárto, B. Z., Lacko, E., Olah, I. & Magyar, A. Characterization of chicken epidermal dendritic cells. Immunology 119, 278–288 (2006)

    Article  Google Scholar 

  28. Winklhofer, M. & Kirschvink, J. Does avian magnetoreception rely on both magnetite and maghemite? http://arxiv.org/abs/0805.2249 (2008)

  29. Walker, M. M. et al. Structure and function of the vertebrate magnetic sense. Nature 390, 371–376 (1997)

    Article  ADS  CAS  Google Scholar 

  30. Horng, Y. M., Wu, C. P., Wang, Y. C. & Huang, M. C. A novel molecular genetic marker for gender determination of pigeons. Theriogenology 65, 1759–1768 (2006)

    Article  CAS  Google Scholar 

  31. Moos, T. & Mollgard, K. A sensitive post-DAB enhancement technique for demonstration of iron in the central nervous system. Histochemistry 99, 471–475 (1993)

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank M. Busslinger, M. Wild and J. Flint for their critical comments on earlier drafts of this manuscript. Thanks also to T. Iancu who commented on our electron micrographs and S. Soto who remarked on the inflammatory lesion in P199. Gratitude is owed to the bio-optics and electron microscopy facilities at the Institute of Molecular Pathology for their assistance in performing experiments. We wish to acknowledge the Centre for Microscopy, Characterisation and Analysis and the Australian Microscopy and Microanalysis Research Facility at the University of Western Australia, a facility funded by the University, State and Commonwealth Governments. Finally, we wish to thank Boehringer Ingelheim, which funds basic science at the Institute of Molecular Pathology.

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Authors and Affiliations

  1. Institute of Molecular Pathology, Dr Bohr-Gasse, Vienna, 1030, Austria

    Christoph Daniel Treiber, Marion Claudia Salzer, Nathaniel Edelman, Cristina Sugar, Martin Breuss, Paul Pichler & David Anthony Keays

  2. Department of Medicine and Institute of Child Health, Centre for Advanced Biomedical Imaging (CABI), University College London (UCL), London WC1E 6DD, UK,

    Johannes Riegler & Mark Lythgoe

  3. Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives (INCI), CNRS UPR 3212, F-67084 Strasbourg, France ,

    Herve Cadiou

  4. Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Crawley, 6009, Australia

    Martin Saunders & Jeremy Shaw

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Contributions

D.A.K. and C.D.T. conceived and designed the study. M.C.S., C.D.T., M.B., P.P., C.S. and N.E., performed the sectioning, PB staining and counting. D.A.K., C.D.T. and H.C. analysed the resultant data. J.R. and M.L. performed the MRI and CT studies, producing the three-dimensional structure of the pigeon beak. D.A.K. performed the immunohistochemical studies. C.D.T performed the ultrastructure experiments and J.S. and M.S. did the EFTEM and SAED studies and analysed the data. D.A.K. wrote the paper, and all authors commented on the manuscript.

Corresponding author

Correspondence to David Anthony Keays.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-17 and Supplementary Tables 1-3. (PDF 9755 kb)

Supplementary Movie 1

This movie shows a three dimensional volume rendering of a pigeon head. Boundaries between skin and air or epithelium and air are shown in purple while the brain and spinal cord are indicated in yellow and the eyes in green. (MOV 7666 kb)

Supplementary Movie 2

This movie shows a series of high resolution magnetic resonance (MRI) images of a pigeon beak co-registered with computed tomography (CT). The movie starts by moving through coronal images along the rostro-caudal axis. Anatomical landmarks are indicated in red on appropriate slices (See Supplementary Figure 5). A surface rendering follows with the MRI data shown in purple, CT yellow data in yellow and landmarks in red. (MOV 8816 kb)

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Treiber, C., Salzer, M., Riegler, J. et al. Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484, 367–370 (2012). https://doi.org/10.1038/nature11046

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