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

Journal of Experimental Biology

Volumn 216, Issue 12, 2013, Pages 2192-2200

  Holland, Richard ^a   Filannino, Caterina ^b   Gagliardo, Anna ^b  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b UNIVERSITY OF PISA   (Italy)

Author keywords

Columba livia; Magnetoreception; Pigeon; True navigation

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; ASSOCIATION; COLUMBA LIVIA; GEOGRAPHIC INFORMATION SYSTEM; ITALY; MAGNETIC FIELD; MAGNETORECEPTION; ORIENTATION; PHYSIOLOGY; PIGEON; PIGEONS AND DOVES; TRUE NAVIGATION;

COLUMBA LIVIA; MAGNETORECEPTION; PIGEON; TRUE NAVIGATION;

ANIMALS; COLUMBIDAE; CUES; GEOGRAPHIC INFORMATION SYSTEMS; HOMING BEHAVIOR; ITALY; MAGNETIC FIELDS; ORIENTATION;

ANIMALIA; AVES; COLUMBA; COLUMBA LIVIA; LAGENA;

EID: 84878547261     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.083543     Document Type: Article

References (64)

1. Able, K. P. (2001). The concepts and terminology of bird navigation. J. Avian Biol. 32, 174-183.
2. Åkesson, S. and Alerstam, T. (1998). Oceanic navigation: are there any feasible geomagnetic bi-coordinate combinations for albatrosses? J. Avian Biol. 29, 618-625.
3. Batschelet, E. (1981). Circular Statistics in Biology. New York: Academic Press.
4. Beason, R. C. and Nichols, J. E. (1984). Magnetic orientation and magnetically sensitive material in a transequatorial migratory bird. Nature 309, 151-153.
5. Beason, R. C. and Semm, P. (1987). Magnetic responses of the trigeminal nerve system of the bobolink (Dolichonyx oryzivorus). Neurosci. Lett. 80, 229-234.
6. Beason, R. C. and Semm, P. (1996). Does the avian ophthalmic nerve carry magnetic navigational information? J. Exp. Biol. 199, 1241-1244.
7. Beason, R. C., Dussourd, N. and Deutschlander, M. E. (1995). Behavioural evidence for the use of magnetic material in magnetoreception by a migratory bird. J. Exp. Biol. 198, 141-146.
8. Beason, R. C., Wiltschko, R. and Wiltschko, W. (1997). Pigeon homing: Effects of magnetic pulses on initial orientation. Auk 114, 405-415.
9. Benhamou, S., Bonadonna, F. and Jouventin, P. (2003). Successful homing of magnet-carrying white-chinned petrels released in the open sea. Anim. Behav. 65, 729-734.
10. Bonadonna, F., Bajzak, C., Benhamou, S., Igloi, K., Jouventin, P., Lipp, H. P. and Dell'Omo, G. (2005). Orientation in the wandering albatross: interfering with magnetic perception does not affect orientation performance. Proc. Biol. Sci. 272, 489-495.
11. Boström, J. E., Åkesson, S. and Alerstam, T. (2012). Where on earth can animals use a geomagnetic bi-coordinate map for navigation? Ecography 35, 1039-1047.
12. Davila, A. F., Winklhofer, M., Shcherbakov, V. P. and Petersen, N. (2005). Magnetic pulse affects a putative magnetoreceptor mechanism. Biophys. J. 89, 56-63.
13. Dennis, T. E., Rayner, M. J. and Walker, M. M. (2007). Evidence that pigeons orient to geomagnetic intensity during homing. Proc. Biol. Sci. 274, 1153-1158.
14. Dunlop, D. (1981). The rock magnetism of fine particles. Phys. Earth Planet. Inter. 26, 1-26.
15. Falkenberg, G., Fleissner, G., Schuchardt, K., Kuehbacher, M., Thalau, P., Mouritsen, H., Heyers, D., Wellenreuther, G. and Fleissner, G. (2010). Avian magnetoreception: elaborate iron mineral containing dendrites in the upper beak seem to be a common feature of birds. PLoS ONE 5, e9231.
16. Fleissner, G., Holtkamp-Rötzler, E., Hanzlik, M., Winklhofer, M., Fleissner, G., Petersen, N. and Wiltschko, W. (2003). Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 458, 350-360.
17. Fleissner, G., Stahl, B., Thalau, P., Falkenberg, G. and Fleissner, G. (2007). A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons. Naturwissenschaften 94, 631-642.
18. Gagliardo, A., Ioalè, P., Savini, M. and Wild, J. M. (2006). Having the nerve to home: trigeminal magnetoreceptor versus olfactory mediation of homing in pigeons. J. Exp. Biol. 209, 2888-2892.
19. Gagliardo, A., Ioalè, P., Savini, M. and Wild, M. (2008). Navigational abilities of homing pigeons deprived of olfactory or trigeminally mediated magnetic information when young. J. Exp. Biol. 211, 2046-2051.
20. Gagliardo, A., Ioalè, P., Savini, M. and Wild, M. (2009). Navigational abilities of adult and experienced homing pigeons deprived of olfactory or trigeminally mediated magnetic information. J. Exp. Biol. 212, 3119-3124.
21. Gagliardo, A., Ioalè, P., Filannino, C. and Wikelski, M. (2011). Homing pigeons only navigate in air with intact environmental odours: a test of the olfactory activation hypothesis with GPS data loggers. PLoS ONE 6, e22385.
22. Griffin, D. R. (1952). Bird navigation. Biol. Rev. Camb. Philos. Soc. 27, 359-390.
23. Harada, Y., Taniguchi, M., Namatame, H. and Iida, A. (2001). Magnetic materials in otoliths of bird and fish lagena and their function. Acta Otolaryngol. 121, 590-595.
24. Henshaw, I., Fransson, T., Jackobsson, S. and Kullberg, C. (2010). Geomagnetic field affects spring migratory direction in a long distance migrant. Behav. Ecol. Sociobiol. 64, 1317-1323.
25. Heyers, D., Zapka, M., Hoffmeister, M., Wild, J. M. and Mouritsen, H. (2010). Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. Proc. Natl. Acad. Sci. USA 107, 9394-9399.
26. Holland, R. A. (2010). Differential effects of magnetic pulses on the orientation of naturally migrating birds. J. R. Soc. Interface 7, 1617-1625.
27. Holland, R. A. and Helm, B. (2013). A strong magnetic pulse affects the precision of departure direction of naturally migrating adult but not juvenile birds. J. R. Soc. Interface 10, 20121047.
28. Holland, R. A., Kirschvink, J. L., Doak, T. G. and Wikelski, M. (2008). Bats use magnetite to detect the Earth's magnetic field. PLoS ONE 3, e1676.
29. Holland, R. A., Thorup, K., Gagliardo, A., Bisson, I. A., Knecht, E., Mizrahi, D. and Wikelski, M. (2009). Testing the role of sensory systems in the migratory heading of a songbird. J. Exp. Biol. 212, 4065-4071.
30. Keeton, W. T. (1974). The orientational and navigational basis of homing in birds. Adv. Stud. Behav. 5, 47-132.
31. Kirschvink, J. L. (1983). Biogenic ferrimagnetism: a new biomagnetism. In Biomagnetism: An Interdisciplinary Approach (ed. S. Williamson), pp. 501-532. New York, NY: Plenum Press.
32. Kirschvink, J. L. (1992). Uniform magnetic fields and double-wrapped coil systems: improved techniques for the design of bioelectromagnetic experiments. Bioelectromagnetics 13, 401-411.
33. Kirschvink, J. L. and Gould, J. L. (1981). Biogenic magnetite as a basis for magnetic field detection in animals. Biosystems 13, 181-201.
34. Kishkinev, D., Mouritsen, H. and Mora, C. V. (2012). An attempt to develop an operant conditioning paradigm to test for magnetic discrimination behavior in a migratory songbird. J. Ornithol. 153, 1165-1177.
35. Lohmann, K. J., Lohmann, C. M. F. and Putman, N. F. (2007). Magnetic maps in animals: nature's GPS. J. Exp. Biol. 210, 3697-3705.
36. Mora, C. V. and Walker, M. M. (2009). Do release-site biases reflect response to the Earth's magnetic field during position determination by homing pigeons? Proc. Biol. Sci. 276, 3295-3302.
37. Mora, C. V., Davison, M., Wild, J. M. and Walker, M. M. (2004). Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432, 508-511.
38. Mouritsen, H. (2012). Sensory biology: search for the compass needles. Nature 484, 320-321.
39. Mouritsen, H. and Hore, P. J. (2012). The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds. Curr. Opin. Neurobiol. 22, 343-352.
40. Mouritsen, H., Huyvaert, K. P., Frost, B. J. and Anderson, D. J. (2003). Waved albatrosses can navigate with strong magnets attached to their head. J. Exp. Biol. 206, 4155-4166.
41. Munro, U., Munro, J. A., Phillips, J. B., Wiltschko, R. and Wiltschko, W. (1997). Evidence for a magnetite-based navigational 'map' in birds. Naturwissenschaften 84, 26-28.
42. Nevitt, G. A. and Bonadonna, F. (2005). Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds. Biol. Lett. 1, 303-305.
43. Papi, F., Fiore, L., Fiaschi, V. and Benvenut, S. (1972). Olfaction and homing in pigeons. Monit. Zool. Ital. 6, 85-95.
44. Phillips, J. B. (1996). Magnetic navigation. J. Theor. Biol. 180, 309-319.
45. Phillips, J. B., Schmidt-Koenig, K. and Muheim, R. (2006). True navigation: sensory bases of gradient maps. In Animal Spatial Cognition: Comparative, Neural, and Computational Approaches (ed. M. F. Brown and R. G. Cook). Available at: www.pigeon.psy.tufts.edu/asc/phillips/.
46. Putman, N. F., Endres, C. S., Lohmann, C. M. F. and Lohmann, K. J. (2011). Longitude perception and bicoordinate magnetic maps in sea turtles. Curr. Biol. 21, 463-466.
47. Semm, P. and Beason, R. C. (1990a). Responses to small magnetic variations by the trigeminal system of the bobolink. Brain Res. Bull. 25, 735-740.
48. Semm, P. and Beason, R. C. (1990b). Responses to small magnetic variations by the trigeminal system of the bobolink. Brain Res. Bull. 25, 735-740.
49. Treiber, C. D., Salzer, M. C., Riegler, J., Edelman, N., Sugar, C., Breuss, M., Pichler, P., Cadiou, H., Saunders, M., Lythgoe, M. et al. (2012). Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484, 367-370.
50. Walcott, C. (1991). Magnetic maps in pigeons. In Orientation in Birds (ed. P. Berthold), pp. 38-51. Basel: Birkhauser-Verlag.
51. Wallraff, H. G. (1972). Homing of pigeons after extirpation of their cochleae and lagenae. Nat. New Biol. 236, 223-224.
52. Wallraff, H. G. (1991). Conceptual approaches to avian navigation. In Orientation in Birds (ed. P. Berthold), pp. 128-165. Basel: Birkhauser.
53. Wallraff, H. G. (2005). Avian Navigation: Pigeon Homing as a Paradigm. Berlin: Springer.
54. Williams, M. N. and Wild, J. M. (2001). Trigeminally innervated iron-containing structures in the beak of homing pigeons, and other birds. Brain Res. 889, 243-246.
55. Wiltschko, R. and Wiltschko, W. (2006). Magnetoreception. Bioessays 28, 157-168.
56. Wiltschko, R. and Wiltschko, W. (2012). The magnetite-based receptors in the beak of birds and their role in avian navigation. J. Comp. Physiol. A 199, 89-98.
57. Wiltschko, W., Munro, U., Beason, R. C., Ford, H. and Wiltschko, R. (1994). A magnetic pulse leads to a temporary deflection in the orientation of migratory birds. Experientia 50, 697-700.
58. Wiltschko, W., Munro, U., Ford, H. and Wiltschko, R. (1998). Effect of a magnetic pulse on the orientation of silvereyes, zosterops l. lateralis, during spring migration. J. Exp. Biol. 201, 3257-3261.
59. Wiltschko, R., Schiffner, I. and Wiltschko, W. (2009a). A strong magnetic anomaly affects pigeon navigation. J. Exp. Biol. 212, 2983-2990.
60. Wiltschko, W., Munro, U., Ford, H. and Wiltschko, R. (2009b). Avian orientation: the pulse effect is mediated by the magnetite receptors in the upper beak. Proc. Biol. Sci. 276, 2227-2232.
61. Wiltschko, R., Schiffer, I., Fuhrmann, P. and Wiltschko, W. (2010). The role of the magnetite based receptors in the beak in pigeon homing. Curr. Biol. 20, 1534-1538.
62. Wu, L.-Q. and Dickman, J. D. (2011). Magnetoreception in an avian brain in part mediated by inner ear lagena. Current Biology 21, 418-423.
63. Wu, L.-Q. and Dickman, J. D. (2012). Neural correlates of a magnetic sense. Science 336, 1054-1057.
64. Zapka, M., Heyers, D., Hein, C. M., Engels, S., Schneider, N.-L., Hans, J., Weiler, S., Dreyer, D., Kishkinev, D., Wild, J. M. et al. (2009). Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461, 1274-1277.