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Magnetoreception and its trigeminal mediation in the homing pigeon

Abstract

Two conflicting hypotheses compete to explain how a homing pigeon can return to its loft over great distances. One proposes the use of atmospheric odours1 and the other the Earth's magnetic field2,3,4 in the ‘map’ step of the ‘map and compass’ hypothesis of pigeon homing5. Although magnetic effects on pigeon orientation6,7 provide indirect evidence for a magnetic ‘map’, numerous conditioning experiments8 have failed to demonstrate reproducible responses to magnetic fields by pigeons. This has led to suggestions that homing pigeons and other birds have no useful sensitivity to the Earth's magnetic field9,10,11. Here we demonstrate that homing pigeons (Columba livia) can discriminate between the presence and absence of a magnetic anomaly in a conditioned choice experiment. This discrimination is impaired by attachment of a magnet to the cere, local anaesthesia of the upper beak area, and bilateral section of the ophthalmic branch of the trigeminal nerve, but not of the olfactory nerve. These results suggest that magnetoreception (probably magnetite-based) occurs in the upper beak area of the pigeon. Traditional methods of rendering pigeons anosmic might therefore cause simultaneous impairment of magnetoreception so that future orientation experiments will require independent evaluation of the pigeon's magnetic and olfactory systems.

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Figure 1: Experimental tunnel used in conditioned choice discrimination of magnetic stimuli.
Figure 2: Percentage of correct choices by four individually trained homing pigeons (P1–P4) discriminating the presence and absence of a magnetic field anomaly over consecutive daily sessions.
Figure 3: Lateral and dorsal (insert) views of the anatomical relationship between the ophthalmic branch (V1) of the trigeminal nerve (NV), the olfactory nerve (NI) and the olfactory mucosa in the head region of the homing pigeon (C. livia).

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Acknowledgements

C.V.M. was formerly Cordula V. Haugh. This work was supported by grants from the Auckland University Research Committee. We thank J. Longville for supplying the pigeons, M. Williams for advice on the use of anaesthetics, B. McArdle for help with statistical analysis, V. Ward for graphical support and R. Mora for technical support.

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Correspondence to Cordula V. Mora.

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Supplementary information

Supplementary Methods

This text describes the pre-training and forced-choice training methods used to prepare four homing pigeons (Columba livia) for the conditioned choice discrimination procedure. It also details the procedure itself, which was used in the baseline and impairment experiments to test individually the magnetic discrimination performance of the pigeons. (DOC 40 kb)

Supplementary Figure 1

This flowchart illustrates the structure of the conditioned choice discrimination procedure used in the baseline and impairment experiments to test individually the magnetic discrimination performance of four homing pigeons (Columba livia). (PDF 23 kb)

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Mora, C., Davison, M., Martin Wild, J. et al. Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432, 508–511 (2004). https://doi.org/10.1038/nature03077

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