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

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.

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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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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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