Testing the role of sensory systems in the migratory heading of a songbird

Journal of Experimental Biology

Volumn 212, Issue 24, 2009, Pages 4065-4071

  Holland, R A ^a,b,g   Thorup, K ^c   Gagliardo, A ^d   Bisson, I A ^b   Knecht, E ^e   Mizrahi, D ^f   Wikelski, M ^b,g  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b PRINCETON UNIVERSITY   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF PISA   (Italy)

^e WAGENINGEN UNIVERSITY   (Netherlands)

^f New Jersey Audubon Society   (United States)

^g MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

Author keywords

Migration; Navigation; Olfaction; Orientation

Indexed keywords

ANIMAL; ARTICLE; FLYING; GEOGRAPHY; MAGNETISM; PHYSIOLOGY; POPULATION MIGRATION; SENSE ORGAN; SONGBIRD; TIME; UNITED STATES;

ANIMAL MIGRATION; ANIMALS; FLIGHT, ANIMAL; GEOGRAPHY; ILLINOIS; MAGNETICS; NEW JERSEY; SENSE ORGANS; SONGBIRDS; TIME FACTORS;

ANIMALIA; AVES; COLUMBA; DUMETELLA; DUMETELLA CAROLINENSIS; PASSERI;

EID: 71849095543     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.034504     Document Type: Article

References (55)

1. Alerstam, T. (1979). Optimal use of wind by migrating birds-combined drift and overcompensation. J. Theor. Biol. 79, 341-353.
2. Alerstam, T. (2006). Conflicting evidence about long-distance animal navigation. Science 313, 791-794.
3. Batschelet, E. (1981). Circular Statistics In Biology. New York: Academic Press.
4. Beason, R. C. and Semm, P. (1996). Does the avian ophthalmic nerve carry magnetic navigational information? J. Exp. Biol. 199, 1241-1244.
5. Beason, R. C., Dussourd, N. and Deutschlander, M. E. (1995). Behavioral evidence for the use of magnetic material in magnetoreception by a migratory bird. J. Exp. Biol. 198, 141-146.
6. Beason, R. C., Wiltschko, R. and Wiltschko, W. (1997). Pigeon homing: Effects of magnetic pulses on initial orientation. Auk 114, 405-415. (Pubitemid 27309109)
7. 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.
8. Benvenuti, S., Fiaschi, V., Fiore, L. and Papi, F. (1973). Homing performances of inexperienced and directionally trained pigeons subjected to olfactory nerve section. J. Comp. Physiol. 83, 81-92.
9. Benvenuti, S., Ioale, P., Gagliardo, A. and Bonadonna, F. (1992). Effects of zinc sulphate-induced anosmia on homing behaviour of pigeons Comp. Biochem. Physiol. 103 A 519-526.
10. Berthold, P. (1991). Spatiotemporal programmes and genetics of orienation. In Orientation In Birds (ed. P. Berthold), pp. 86-105. Basel: Birkhauser Verlag.
11. Berthold, P. (2001). Bird Migration: A General Survey. Oxford: Oxford University Press.
12. Bingman, V. P. and Cheng, K. (2006). Mechanisms of animal global navigation: Comparative perspectives and enduring challenges. Ethol. Ecol. Evol. 17, 295-318.
13. 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. R. Soc. Lond. B 272, 489-495.
14. Cancalon, P. (1982). Degeneration and regeneration of olfactory cells induced by ZnSO4 and other chemicals. Tissue Cell 14, 717-733.
15. Chernetsov, N., Kishkinev, D. and Mouritsen, H. (2008). A long distance avian migrant compensates for longitudinal displacement during spring migration. Curr. Biol. 18, 188-190.
16. Dunlop, D. (1981). The rock magnetism of fine particles. Phys. Earth Planet Int. 26, 1-26.
17. Fiaschi, V., Farina, M. and Ioale, P. (1974). Homing experiments on swifts Apus apus deprived of olfactory perception. Monitore Zool. Ital. 8, 235-244.
18. Fischer, J., Munro, U. and Phillips, J. B. (2003). Magnetic navigation by an avian migrant? In Avian migration (ed. P. Berthold, E. Gwinner and E. Sonnenschein), pp. 423-432. Heidelberg and New York: Springer-Verlag.
19. Fleissner, G., Holtkamp-Rotzler, E., Hanzlik, M., Winklhofer, M., Petersen, N. and Wiltschko, W. (2003). Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 458, 350-360.
20. Gagliardo, A., Fiaschi, V. and Benvenuti, S. (1988). Pigeon homing: olfactory experiments with young ineperienced birds Naturwiss. 75, 211-213.
21. Gagliardo, A., Ioale, 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.
22. Gagliardo, A., Ioale, P., Savini, M. and Wild, J. M. (2008). Navigational abilities of homing pigeons deprived of olfactory or trigeminally mediated magnetic information when young. J. Exp. Biol. 211, 2046-2051.
23. Griffin, D. R. (1952). Bird Navigation. Biol. Rev. Cam. Phil. Soc. 27, 359-393.
24. Hagstrum, J. T. (2000). Infrasound and the avian navigational map. J. Exp. Biol. 203, 1103-1111.
25. Hagstrum, J. T. (2001). Infrasound and the avian navigational map. J. Nav. 54, 377-391.
26. 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.
27. Jorge, P. E., Marques, A. E. and Phillips, J. B. (2009a). Activation rather than navigational effects of odours on homing of young pigons. Curr. Biol. 19, 1-5.
28. Jorge, P. E., Marques, A. E. and Phillips, J. B. (2009b). Activation effects of odours on avian navigation. Proc. R. Soc. Lond. B. doi:10.1098/rspb.2009.1521.
29. Kirschvink, J. L. (1983). Biogenic ferrimagnetism: a new biomagnetism. In Biomagnetism: An Interdisciplinary Approach (ed. S. Williamson), pp. 501-532. New York: Plenum Press.
30. Kirschvink, J. L. (1992). Uniform magnetic-fields and double-wrapped coil systems-improved techniques for the design of bioelectromagnetic experiments. Bioelectromagnetics 13, 401-411.
31. Kirschvink, J. L., Walker, M. M. and Diebel, C. E. (2001). Magnetite based magnetoreception. Curr. Opin. Neurobiol. 11, 462-467.
32. Matthews, G. V. T. (1953). Sun navigation in homing pigeons. J. Exp. Biol. 30, 243-267.
33. 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. (Pubitemid 39576532)
34. 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.
35. Munro, U., Munro, J. A., Phillips, J. B. and Wiltschko, W. (1997a). Effect of wavelength of light and pulse magnetisation on different magnetoreception systems in a migratory bird. Aust. J. Zool. 45, 189-198.
36. Munro, U., Munro, J. A., Phillips, J. B., Wiltschko, R. and Wiltschko, W. (1997b). Evidence for a magnetite-based navigational 'map' in birds. Naturwiss. 84, 26-28.
37. Newton, I. (2007). The Migration Ecology Of Birds. London: Academic Press.
38. Papi, F. (2001). Animal navigation at the end of the century: a retrospect and a look forward. It. J. Zool. 68, 171-180.
39. Papi, F., Fiore, L., Fiaschi, V. and Benvenutii, S. (1973). Experiment for testing hypothesis of olfactory navigation of homing pigeons. J. Comp. Physiol. 83, 93-102.
40. Pennycuick, C. J. (1960). Sun navigation in birds - reply. Nature 188, 1127-1128.
41. Perdek, A. C. (1958). Two types of orientation in migrating Sturnus vulgarisand Fringilla coelebs. Ardea 46, 1-37.
42. Phillips, J. B. (1996). Magnetic navigation. J. Theor. Biol. 180, 309-319.
43. 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). www.pigeon.psy.tufts.edu/asc/phillips/.
44. Sauer, E. G. F. and Sauer, E. M. (1960). Star navigation of nocturnal migrating birds-the 1958 planetarimum experiments. Cold Spring Harb. Symp. Quant. Biol.25, 463-473.
45. Stutchbury, B. J. M., Tarof, S. A., Done, T., Gow, E., Kramer, P. M., Tautin, J., Fox, J. W. and Afanasyev, V. (2009). Tracking long-distance songbird migration by using geolocators. Science 323, 896.
46. Thorup, K., Alerstam, T., Hake, M. and Kjellén, N. (2003). Bird orientation: compensation for wind drift in migrating raptors is age dependent. Proc. R. Soc. Lond. B 270, S8-S11.
47. Thorup, K., Bisson, I., Bowlin, M., Holland, R. A., Ramenofsky, M., Wingfield, J. and Wikelski, M. (2007). Migration routes of adult and juvenile white-crowned sparrows differ after continent-wide displacement during migration. Proc. Natl. Acad. Sci. USA 104, 18115-18119.
48. Wallraff, H. G. (2005). Avian Navigation: Pigeon Homing As A Paradigm. Berlin: Springer.
49. Wallraff, H. G., Kiepenheuer, J., Neumann, M. F. and Streng, A. (1995). Homing experiments with starlings deprived of the sense of smell. Condor 97, 20-26.
50. Wikelski, M., Kays, R. W., Kasdin, N. J., Thorup, K., Smith, J. A. and Swenson, G. W. (2007). Going wild: what a global small-animal tracking system could do for experimental biologists. J. Exp. Biol. 210, 181-186.
51. Wiltschko, R. and Wiltschko, W. (2003). Mechanisms of orientation and navigation in migratory birds. In Avian Migration (ed. P. Berthold, E. Gwinner and E. Sonnenschein), pp. 433-456. Berlin: Springer.
52. Wiltschko, W. and Wiltschko, R. (1995). Migratory orientation of european robins is affected by the wavelength of light as well as by a magnetic pulse. J. Comp. Physiol. A. Neural Behav. Physiol. 177, 363-369.
53. 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. (Pubitemid 24234375)
54. 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.
55. Wiltschko, W., Munro, U., Ford, H. and Wiltschko, R. (2006). Bird navigation: what type of information does the magnetite-based receptor provide. Proc. R. Soc. Lond. B273, 2815-2820.