Avian Magnetoreception: Elaborate Iron Mineral Containing Dendrites in the Upper Beak Seem to Be a Common Feature of Birds

Falkenberg, Gerald; Schuchardt, K.; Kuehbacher, M.; Thalau, Peter; Mouritsen, Henrik; Heyers, Dominik; Wellenreuther, Gerd; Fleissner, Gerta

doi:10.1371/journal.pone.0009231

Cited by 122 publications

(114 citation statements)

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“…More direct methods, such as electrophysiological recordings from trigeminal neurons in response to magnetic stimulation, would be required to prove this; however, as pointed out earlier here, such methods are very prone to the production of artifactual results (22-24); hence, the necessity for the present, strongly indicative study using more indirect methods. The data also suggest that the ophthalmic branch of the trigeminal nerve (V1) in European robins innervates a primary magnetic sensor in the upper beak and support the idea that iron-mineral-based structures found in the upper beak of birds (8,12,13) including European robins (15), can sense information from the ambient geomagnetic field.…”

Section: Discussionsupporting

confidence: 69%

“…In recent years, mounting behavioral and anatomical evidence has been accumulating that birds, at least, might have two independent magnetic senses: (i) iron-mineral-based sensors located in the upper beak, which are innervated by the ophthalmic branch of the trigeminal nerve (V1) (8,9,(11)(12)(13)(14)(15)(16), and (ii) a light-dependent chemical sense which is embedded in parts of the visual system (7,9,(16)(17)(18)(19)(20)(21). However, considerable scientific skepticism remains regarding both of these proposed magnetic senses because, so far, in birds, the studies that have reported changes in neurophysiological activity in response to magnetic field changes differ in their conclusions, could not be independently confirmed, and are likely to have been subject to artifactual difficulties (22)(23)(24).…”

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confidence: 99%

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Magnetic field changes activate the trigeminal brainstem complex in a migratory bird

Heyers

Zapka

Hoffmeister

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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The upper beak of birds, which contains putative magnetosensory ferro-magnetic structures, is innervated by the ophthalmic branch of the trigeminal nerve (V1). However, because of the absence of replicable neurobiological evidence, a general acceptance of the involvement of the trigeminal nerve in magnetoreception is lacking in birds. Using an antibody to ZENK protein to indicate neuronal activation, we here document reliable magnetic activation of neurons in and near the principal (PrV) and spinal tract (SpV) nuclei of the trigeminal brainstem complex, which represent the two brain regions known to receive primary input from the trigeminal nerve. Significantly more neurons were activated in PrV and in medial SpV when European robins (Erithacus rubecula) experienced a magnetic field changing every 30 seconds for a period of 3 h (CMF) than when robins experienced a compensated, zero magnetic field condition (ZMF). No such differences in numbers of activated neurons were found in comparison structures. Under CMF conditions, sectioning of V1 significantly reduced the number of activated neurons in and near PrV and medial SpV, but not in lateral SpV or in the optic tectum. Tract tracing of V1 showed spatial proximity and regional overlap of V1 nerve endings and ZENK-positive (activated) neurons in SpV, and partly in PrV, under CMF conditions. Together, these results suggest that magnetic field changes activate neurons in and near the trigeminal brainstem complex and that V1 is necessary for this activation. We therefore suggest that V1 transmits magnetic information to the brain in this migratory passerine bird.bird migration | magnetic sense | magnetite | magnetoperception | magnetoreception

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Section: Discussionsupporting

confidence: 69%

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confidence: 99%

Magnetic field changes activate the trigeminal brainstem complex in a migratory bird

Heyers

Zapka

Hoffmeister

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

118

124

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“…Several groups have attempted to identify the primary sensory cells associated with an iron oxide-based magnetoreceptor (19)(20)(21)(22)(23)(24). Most have used the Prussian Blue reaction which labels ferric iron.…”

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confidence: 99%

No evidence for intracellular magnetite in putative vertebrate magnetoreceptors identified by magnetic screening

Edelman

Fritz

Nimpf

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The cellular basis of the magnetic sense remains an unsolved scientific mystery. One theory that aims to explain how animals detect the magnetic field is the magnetite hypothesis. It argues that intracellular crystals of the iron oxide magnetite (Fe3O4) are coupled to mechanosensitive channels that elicit neuronal activity in specialized sensory cells. Attempts to find these primary sensors have largely relied on the Prussian Blue stain that labels cells rich in ferric iron. This method has proved problematic as it has led investigators to conflate iron-rich macrophages with magnetoreceptors. An alternative approach developed by Eder et al. [Eder SH, et al. (2012) Proc Natl Acad Sci USA 109(30):12022–12027] is to identify candidate magnetoreceptive cells based on their magnetic moment. Here, we explore the utility of this method by undertaking a screen for magnetic cells in the pigeon. We report the identification of a small number of cells (1 in 476,000) with large magnetic moments (8–106 fAm2) from various tissues. The development of single-cell correlative light and electron microscopy (CLEM) coupled with electron energy loss spectroscopy (EELS) and energy-filtered transmission electron microscopy (EFTEM) permitted subcellular analysis of magnetic cells. This revealed the presence of extracellular structures composed of iron, titanium, and chromium accounting for the magnetic properties of these cells. Application of single-cell CLEM to magnetic cells from the trout failed to identify any intracellular structures consistent with biogenically derived magnetite. Our work illustrates the need for new methods to test the magnetite hypothesis of magnetosensation.

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“…Initially, iron-containing cells found in the upper beak of homing pigeons and other birds (Beason and Nichols, 1984;Falkenberg et al, 2010;Fleissner et al, 2003;Fleissner et al, 2007;Williams and Wild, 2001) were suggested as magnetoreceptors innervated via the V1. However, a recent and thorough study made on homing pigeons (Treiber et al, 2012) strongly suggested that the majority, if not all, of Fe-positive cells both in the upper beak and other parts, such as skin, respiratory epithelium and feathers folliculi, are represented by macrophages.…”

Section: Introductionmentioning

confidence: 99%

A magnetic pulse does not affect homing pigeon navigation: a GPS tracking experiment

Holland

Filannino

Gagliardo

2013

Journal of Experimental Biology

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SUMMARYThe cues by which homing pigeons are able to return to a home loft after displacement to unfamiliar release sites remain debated. A number of experiments in which migratory birds have been treated with a magnetic pulse have produced a disruption in their orientation, which argues that a ferrimagnetic sense is used for navigation in birds. One previous experiment has also indicated an effect of magnetic pulses on homing pigeon navigation, although with inconsistent results. Previous studies have shown that some magnetic-related information is transmitted by the trigeminal nerve to the brain in some bird species, including the homing pigeon. The function of this information is still unclear. It has been suggested that this information is important for navigation. Previous studies with trigeminal nerve lesioned homing pigeons have clearly shown that the lack of trigeminally mediated information, even if magnetic, is not crucial for homing performance. However, this result does not completely exclude the possibility that other ferrimagnetic receptors in the homing pigeon play a role in navigation. Additionally, recent studies on homing pigeons suggested the existence of a ferrimagnetic sense in a novel location presumably located in the inner ear (lagena). In the present study, we tested whether any ferrimagnetic magnetoreceptors, irrespective of their location in the birdʼs head, are involved in pigeonsʼ homing. To do this, we treated homing pigeons with a strong magnetic pulse before release, tracked birds with GPS loggers and analyzed whether this treatment affected homing performance. In the single previous magnetic pulse experiment on homing pigeons, only initial orientation at a release site was considered and the results were inconsistent. We observed no effect of the magnetic pulse at any of the sites used on initial orientation, homing performance, tortuosity or track efficiency, which does not support a role for the ferrimagnetic sense in homing pigeon navigation, at least not in this geographic area, where magnetic field variations are in the region of 200nT intensity and 0.8deg inclination. Supplementary material available online at

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Avian Magnetoreception: Elaborate Iron Mineral Containing Dendrites in the Upper Beak Seem to Be a Common Feature of Birds

Cited by 122 publications

References 49 publications

Magnetic field changes activate the trigeminal brainstem complex in a migratory bird

Magnetic field changes activate the trigeminal brainstem complex in a migratory bird

No evidence for intracellular magnetite in putative vertebrate magnetoreceptors identified by magnetic screening

A magnetic pulse does not affect homing pigeon navigation: a GPS tracking experiment

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