True navigation in birds: From quantum physics to global migration

Journal of Zoology

Volumn 293, Issue 1, 2014, Pages 1-15

  Holland, R A ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Bird; Magnetoreception; Map; Migration; Navigation; Olfaction; Orientation

Indexed keywords

ANIMALIA; AVES;

EID: 84899919462     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/jzo.12107     Document Type: Article

References (152)

1. Able, K.P. (2001). The concepts and terminology of bird navigation. J. Av. Biol. 32, 174-183.
2. Able, K.P. & Cherry, J.D. (1986). Mechanisms of dusk orientation in white-throated sparrows (Zonotrichia albicollis): clock-shift experiments. J. Comp. Physiol. [A.] 159, 107-113.
3. Able, K.P. & Dillon, P.M. (1977). Sun compass orientation in a nocturnal migrant white throated sparrow. Condor 79, 393-395.
4. Alerstam, T. (2006). Conflicting evidence about long-distance animal navigation. Science 313, 791-794.
5. Åkesson, S., Morin, J., Muheim, R. & Ottosson, U. (2005). Dramatic orientation shift of white-crowned sparrows displaced across longitudes in the high arctic. Curr. Biol. 15, 1591-1597.
6. Baker, R.R. (1984). Bird navigation: the solution of a mystery?. London: Hodder Arnold.
7. Baldaccini, N.E., Benvenuti, S., Fiaschi, V. & Papi, F. (1975). Pigeon navigation - effects of wind deflection at home cage on homing behavior. J. Comp. Physiol. 99, 177-186.
8. Beason, R.C. & Nichols, J.E. (1984). Magnetic orientation and magnetically sensitive material in a transequatorial migratory bird. Nature 309, 151-153.
9. Beason, R.C. & Semm, P. (1996). Does the avian ophthalmic nerve carry magnetic navigational information? J. Exp. Biol. 199, 1241-1244.
10. Beason, R.C., Dussourd, N. & Deutschlander, M.E. (1995). Behavioral evidence for the use of magnetic material in magnetoreception by a migratory bird. J. Exp. Biol. 198, 141-146.
11. Beason, R.C., Wiltschko, R. & Wiltschko, W. (1997). Pigeon homing: effects of magnetic pulses on initial orientation. Auk 114, 405-415.
12. Beck, W. & Wiltschko, W. (1988). Magnetic factors control the migratory direction of Pied Flycatchers (Ficedula hypoleuca Pallas), In Acta 19th congress internationa ornithology, Vol. II, 1955-1962. Ouellet, H. (Ed.). Ottawa:University of Ottawa Press.
13. Benhamou, S., Bonadonna, F. & Jouventin, P. (2003). Successful homing of magnet-carrying white-chinned petrels released in the open sea. Anim. Behav. 65, 729-734.
14. Benvenuti, S. & Wallraff, H.G. (1985). Pigeon navigation: site simulation by means of atmospheric odours. J. Comp. Physiol. [A.] 156, 737-746.
15. Benvenuti, S., Fiaschi, V., Fiore, L. & Papi, F. (1973). Homing performances of inexperienced and directionally trained pigeons subjected to olfactory nerve section. J. Comp. Physiol. 83, 81-92.
16. Bingman, V.P. & Cheng, K. (2006). Mechanisms of animal global navigation: comparative perspectives and enduring challenges. Ethol. Ecol. Evol. 17, 295-318.
17. Biskup, T., Schleicher, E., Okafuji, A., Link, G., Hitomi, K., Getzoff, E.D. & Weber, S. (2009). Direct observation of a photoinduced radical pair in a cryptochrome blue-light photoreceptor. Angew Chem Int Ed 48, 404-407.
18. Blakemore, R.P. (1975). Magnetotactic bacteria. Science 190, 377-379.
19. Bonadonna, F., Bajzak, C., Benhamou, S., Igloi, K., Jouventin, P., Lipp, H.P. & 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.
20. Boström, J.E., Åkesson, S. & Alerstam, T. (2012). Where on earth can animals use a geomagnetic bi-coordinate map for navigation? Ecography 35, 1039-1047.
21. Bouly, J.-P., Schleicher, E., Dionisio-Sese, M., Vandenbussche, F., Van Der Straeten, D., Bakrim, N., Meier, S., Batschauer, A., Galland, P., Bittl, R. & Ahmad, M. (2007). Cryptochrome blue light photoreceptors are activated through interconversion of flavin redox states. J. Biol. Chem. 282, 9383-9391.
22. Bridge, E.S., Thorup, K., Bowlin, M.S., Chilson, P.B., Diehl, R., Fleron, R.W., Hartl, P., Kays, R.W., Kelly, J.F., Robinson, W.D. & Wikelksi, M. (2011). Technology on the move: recent and forthcoming innoviations for tracking migratory birds. Biosci. 61, 689-698.
23. Chernetsov, N., Kishkinev, D. & Mouritsen, H. (2008). A long distance avian migrant compensates for longitudinal displacement during spring migration. Curr. Biol. 18, 188-190.
24. Dennis, T.E., Rayner, M.J. & Walker, M.M. (2007). Evidence that pigeons orient to geomagnetic intensity during homing. Proc. R. Soc. Lond. B. 274, 1153-1158.
25. Deutchlander, M.E., Phillips, J.B. & Munro, U. (2012). Age-dependent orientation to magnetically-simulated geographic displacements in migratory Australian silvereyes (Zosterops l. lateralis). Wilson J Ornithol. 124, 467-477.
26. Dingle, H. (1996). Migration: the biology of life on the move. London: Lightning Source.
27. Emlen, S.T. (1967). Migratory orientation in indigo bunting Passerina Cyanea. Part II: mechanisms of celestial navigation. Auk 84, 463-489.
28. Emlen, S.T. & Emlen, J.T. (1966). A technique for recording migratory orientation of captive birds. Auk 83, 361-367.
29. Falkenberg, G., Fleissner, G., Schuchardt, K., Kuehbacher, M., Thalau, P., Mouritsen, H., Heyers, D., Wellenreuther, G. & 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.
30. Fiaschi, V., Farina, M. & Ioalé, P. (1974). Homing experiments on swifts Apus apus (L.) deprived of olfactory perception. Monitore Zoologica Italiano 8, 235-244.
31. Fischer, J., Munro, U. & Phillips, J.B. (2003). Magnetic navigation by an avian migrant?, In Avian migration: 423-432. Berthold, P., Gwinner, E. & Sonnenschein, E. (Eds). Heidelberg-New York: Springer-Verlag.
32. Fischer, J.H., Freake, M.J., Borland, S.C. & Phillips, J.B. (2001). Evidence for the use of magnetic map information by an amphibian. Anim. Behav. 62, 1-10.
33. Fleissner, G., Holtkamp-Rotzler, E., Hanzlik, M., Winklhofer, M., Petersen, N. & Wiltschko, W. (2003). Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 458, 350-360.
34. Foa, A., Bagnoli, P. & Giongo, F. (1986). Homing pigeons subjected to section of the anterior commissure can build up 2 olfactory maps in the deflector lofts. J. Comp. Physiol. [A.] 159, 465-472.
35. Fransson, T., Jakobsson, S., Johansson, P., Kullberg, C., Lind, J. & Vallin, A. (2001). Bird migration: magnetic cues trigger extensive refuelling. Nature 414, 35-36.
36. Gagliardo, A., Ioale, P., Odetti, F. & Bingman, V.P. (2001). The ontogeny of the homing pigeon navigational map: evidence for a sensitive learning period. Proc. R. Soc. Lond. B 268, 197-202.
37. Gagliardo, A., Ioale, P., Savini, M. & Wild, J.M. (2006). Having the nerve to home: trigeminal magnetoreceptor versus olfactory mediation of homing in pigeons. J. Exp. Biol. 209, 2888-2892.
38. Gagliardo, A., Ioale, P., Savini, M. & 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.
39. Gagliardo, A., Ioale, P., Savini, M. & Wild, J.M. (2009). Navigational abilities of adult and experienced homing pigeons deprived of olfactory or trigeminally mediated magnetic information. J. Exp. Biol. 212, 3119-3124.
40. Gagliardo, A., Ioale, P., Filannino, C. & 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.
41. Griffin, D.R. (1952). Bird navigation. Biol. Rev. 27, 359-400.
42. Guilford, T., Akesson, S., Gagliardo, A., Holland, R.A., Mouritsen, H., Muheim, R., Wiltschko, R., Wiltschko, W. & Bingman, V.P. (2011). Migratory navigation in birds: new opportunities in an era of fast-developing tracking technology. J. Exp. Biol. 214, 3705-3712.
43. Hagstrum, J.T. (2000). Infrasound and the avian navigational map. J. Exp. Biol. 203, 1103-1111.
44. Hagstrum, J.T. (2001). Infrasound and the avian navigational map. J. Nav. 54, 377-391.
45. Hagstrum, J.T. (2013). Atmospheric propagation modelling indicates homing pigeons use loft-specific infrasonic 'map' cues. J. Exp. Biol. 216, 687-699.
46. Hein, C.M., Engels, S., Kishkinev, D. & Mouritsen, H. (2011). Robins have a magnetic compass in both eyes. Nature 471, E11-E12.
47. Henshaw, I., Fransson, T., Jackobsson, S. & Kullberg, C. (2010). Geomagnetic field affects spring migratory direction in a long distance migrant. Behav. Ecol. Sociobiol. 64, 1317-1323.
48. Heyers, D., Zapka, M., Hoffmeister, M., Wild, J.M. & Mouritsen, H. (2010). Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. Proc. Nat. Acad. Sci. U.S.A. 107, 9394-9399.
49. Holland, R. & Helm, B. (2013). A magnetic pulse affects the precision of departure direction of naturally migrating adult but not juvenile birds. J. R. Soc. Int. 10, 20121047.
50. Holland, R.A. (2010). Differential effects of magnetic pulses on the departure directions of naturally migrating birds. J. R. Soc. Int. 7, 1617-1625.
51. Holland, R.A., Thorup, K. & Wikelski, M. (2007). Where the wild things go. Biologist 54, 214-219.
52. Holland, R.A., Thorup, K., Gagliardo, A., Bisson, I., Knecht, E., Mizrahi, D. & Wikelski, M. (2009). Testing the role of sensory systems in the migratory heading of a songbird. J. Exp. Biol. 212, 4065-4071.
53. Ioale, P., Papi, F., Fiaschi, V. & Baldaccini, N.E. (1978). Pigeon navigation: effects of homing behaviour by reversing wind direction at the loft. J. Comp. Physiol. 128, 285-295.
54. Ioale, P., Nozzolini, M. & Papi, F. (1990). Homing pigeons do extract directional information from olfactory stimuli. Behav. Ecol. Sociobiol. 26, 301-305.
55. Jacobs, L.F. (2012). From chemotaxis to the cognitive map: the function of olfaction. Proc. Nat. Acad. Sci. U.S.A. 109, 10693-10700.
56. Jorge, P.E., Marques, A.E. & Phillips, J.B. (2009). Activation rather than navigational effects of odours on homing of young pigons. Curr. Biol. 19, 1-5.
57. Jorge, P.E., Marques, A.E. & Phillips, J.B. (2010). Activation effects of odours on avian navigation. Proc. R. Soc. Lond. B 277, 45-49.
58. Keeton, W.T. (1974). The orientational and navigational basis of homing in birds. Adv Stud Behav. 5, 47-132.
59. Kennedy, D. & Norman, C. (2005). What don't we know? Science Special Issue 309, 1-204.
60. Kirschvink, J.L. (1982). Birds, bees and magnetism - a new look at the old problem of magnetoreception. Trends Neurosci. 5, 160-167.
61. Kirschvink, J.L. & Gould, J.L. (1981). Biogenetic magnetite as a basis for magnetic field detection in animals. Biosystems 13, 181-201.
62. Kirschvink, J.L. & Walker, M.M. (1985). Particle-size considerations for magnetite based magnetoreceptors, In Magnetite biomineralization and magnetoreception in organisms: 243-254. Kirschvink, J.L., Jones, D.S. & MacFadden, B.J. (Eds). New York: Plenum Press.
63. Kirschvink, J.L., Walker, M.M., Chang, S.B., Dizon, A.E. & Peterson, K.A. (1985). Chains of single domain magnetite particles in chinook salmon, Onchorhynchus tshawytscha. J. Comp. Physiol. [A.] 157, 375-381.
64. Kirschvink, J.L., Winklhofer, M. & Walker, M.M. (2010). Biophysics of magnetic orientation: strengthening the interface between theory and experimental design. J. R. Soc. Int. doi: 10.1098/rsif.2009.0491.focus.
65. Kishkinev, D., Chernetsov, N. & Mouritsen, H. (2010). A double clock or jetlag mechanism is unlikely to be involved in detection of east-west displacements in a long distance avian migrant. Auk 127, 773-780.
66. Kishkinev, D., Mouritsen, H. & Mora, C.V. (2012). An attempt to develop an operant conditioning paradigm to test for magnetic discrimination behavior in a migratory songbird. J. Orn. 153, 1165-1177.
67. Kishkinev, D., Chernetsov, N., Heyers, D. & Mouritsen, H. (2013). Migratory reed warblers need intact trigeminal nerves to correct for a 1000km eastward displacement. PLoS ONE 8, e65847.
68. Kramer, G. (1953). Wird die Sonnehöhe bei der Heimfindeorientierung verwertet? J. Orn. 94, 201-219.
69. Lauwers, M., Pichler, P., Edelman, N.B., Resch, G.P., Ushakova, L., Salzer, M.C., Heyers, D., Saunders, M., Shaw, J. & Keays, D.A. (2013). An iron-rich organelle in the cuticular plate of avian hair cells. Curr. Biol. 23, 924-929.
70. Liedvogel, M. & Mouritsen, H. (2010). Cryptochromes-a potential magnetoreceptor: what do we know and what do we want to know? J. R. Soc. Int. 7, S147-S162.
71. Liedvogel, M., Maeda, K., Henbest, K., Schleicher, E., Simon, T., Timmel, C.R., Hore, P.J. & Mouritsen, H. (2007). Chemical magnetoreception: bird cryptochrome 1a is excited by blue light and forms long-lived radical-pairs. PLoS ONE 2, doi: 10.1371/journal.pone.0001106.
72. Lohmann, K.J., Pentcheff, N.D., Nevitt, G.A., Stetten, G.D. & Zimmer-Faust, R.K. (1995). Magnetic orientation of spiny lobsters in the ocean: experiments with underseas coil systems. J. Exp. Biol. 198, 2041-2048.
73. Lohmann, K.J., Lohmann, C.M.F., Ehrhart, L.M., Bagley, D.A. & Swing, T. (2004). Geomagnetic map used in sea turtle navigation. Nature 428, 909-910.
74. Maeda, K., Robinson, A.J., Henbest, K.B., Hogben, H.J., Biskup, T., Ahmad, M., Schleicher, E., Weber, S., Timmel, C.R. & Hore, P.J. (2012). Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor. Proc. Nat. Acad. Sci. U.S.A. 109, 4774-4779.
75. Matthews, G.V.T. (1951). The experimental investigation of navigation in homing pigeons. J. Exp. Biol. 28, 508-536.
76. Matthews, G.V.T. (1953). Sun navigation in homing pigeons. J. Exp. Biol. 30, 243-267.
77. Merkel, F.W. & Wiltschko, W. (1965). Magnetismus und richtungsfinden zugunruhiger rotkehlchen (Erithacus rubecula). Vogelwarte 23, 71-77.
78. Mewaldt, L.R., Cowley, L.T. & Won, P.O. (1973). Californian sparrows fail to return from displacement to Korea. Auk 90, 857-861.
79. Moller, A., Sagasser, S., Wiltschko, W. & Schierwater, B. (2004). Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass. Naturwiss. 91, 585-588.
80. Mora, C.V. & Walker, M.M. (2009). Do release-site biases reflect response to the Earth's magnetic field during position determination by homing pigeons? Proc. R. Soc. Lond. B 276, 3295-3302.
81. Mora, C.V., Davison, M., Wild, J.M. & Walker, M.M. (2004). Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432, 508-511.
82. Mouritsen, H. (2012). Sensory biology search for the compass needles. Nature 484, 320-321.
83. Mouritsen, H. & Hore, P.J. (2012). The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds. Curr. Opin. Neurobiol. 22, 343-352.
84. Mouritsen, H. & Larsen, O.N. (2001). Migrating songbirds tested in computer-controlled Emlen funnels use stellar cues for a time-independent compass. J. Exp. Biol. 204, 3855-3865.
85. Mouritsen, H., Huyvaert, K.P., Frost, B.J. & Anderson, D.J. (2003). Waved albatrosses can navigate with strong magnets attached to their head. J. Exp. Biol. 206, 4155-4166.
86. Mouritsen, H., Janssen-Bienhold, U., Liedvogel, M., Feenders, G., Stalleicken, J., Dirks, P. & Weiler, R. (2004). Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proc. Nat. Acad. Sci. U.S.A. 101, 14294-14299.
87. Mouritsen, H., Feenders, G., Liedvogel, M., Wada, K. & Jarvis, E.D. (2005). A night vision brain area in migratory songbirds. Proc. Natl Acad. Sci. USA 102, 8339-8344.
88. Muheim, R. & Akesson, S. (2002). Clock-shift experiments with Savannah sparrows, passerculus sandwichensis, at high northern latitudes. Behav. Ecol. Sociobiol. 51, 394-401.
89. Munro, U. & Wiltschko, R. (1993). Clock shift experiments with migratory yellow faced honeyeaters, Lichenostomus crysops (Meliphagidae), and australian day migrating bird. J. Exp. Biol. 181, 233-244.
90. Munro, U., Munro, J.A., Phillips, J.B., Wiltschko, R. & Wiltschko, W. (1997a). Evidence for a magnetite-based navigational 'map' in birds. Naturwiss. 84, 26-28.
91. Munro, U., Munro, J.A., Phillips, J.B. & Wiltschko, W. (1997b). Effect of wavelength of light and pulse magnetisation on different magnetoreception systems in a migratory bird. Aust. J. Zool. 45, 189-198.
92. Newton, I. (2007). The migration ecology of birds: London: Academic Press.
93. Niessner, C., Denzau, S., Gross, J.C., Peichl, L., Bischof, H.-J., Fleissner, G., Wiltschko, W. & Wiltschko, R. (2011). Avian ultraviolet/violet cones identified as probable magnetoreceptors. PLoS ONE 6, e20091.
94. Papi, F. (1992). General aspects, In Animal homing: 1-18. Papi, F. (Ed.). London: Chapman Hall.
95. Pennycuick, C.J. (1960). The physical basis of astronavigation in birds: theoretical considerations. J. Exp. Biol. 37, 573-593.
96. Pennycuick, C.J. (1961). Sun navigation in birds? Nature 190, 1127-1128.
97. Perdeck, A.C. (1958). Two types of orientation in migrating Sturnus vulgaris and Fringilla coelebs. Ardea 46, 1-37.
98. Perdeck, A.C. (1967). Orientation of starlings after displacement to Spain. Ardea 55, 194-202.
99. Phillips, J.B. (1996). Magnetic navigation. J. Theor. Biol. 180, 309-319.
100. Phillips, J.B. & Waldvogel, J.A. (1982). Reflected light cues generate the short-term deflector loft effect, In Avian navigation: 190-202. Papi, F. & Wallraff, H.G. (Eds). Berlin: Springer.
101. Phillips, J.B., Schmidt-Koenig, K. & Muheim, R. (2006). True navigation: sensory bases of gradient maps, In Animal spatial cognition: comparative, neural, and computational approaches. Brown, M.F. & Cook, R.G. (Eds). Available:: www.pigeon.psy.tufts.edu/asc/phillips/.
102. Putman, N.F., Endres, C.S., Lohmann, C.M.F. & Lohmann, K.J. (2011). Longitude perception and bicoordinate magnetic maps in sea turtles. Curr. Biol. 21, 463-466.
103. Rastogi, A., Kumari, Y., Rani, S. & Kumar, V. (2011). Phase inversion of neural activity in the olfactory and visual systems of a night-migratory bird during migration. Eur. J. Neurosci. 34, 99-109.
104. Ritz, T., Adem, S. & Schulten, K. (2000). A model for vision based magnetoreception in birds. Biophys. J. 78, 707-718.
105. Ritz, T., Thalau, P., Phillips, J.B., Wiltschko, R. & Wiltschko, W. (2004). Resonance effects indicate radical pair mechanism for avian magnetic compass. Nature 429, 177-180.
106. Rogers, C.T. & Hore, P.J. (2009). Chemical magnetoreception in birds: the radical pair mechanism. Proc. Nat. Acad. Sci. U.S.A. 106, 353-360.
107. Schmidt-Koenig, K. (1960). The sun azimuth compass: one factor in the orientation of homing pigeons. Science (New York, N.Y.) 131, 826-827.
108. Schmidt-Koenig, K., Ganzhorn, J.U. & Ranvaud, R. (1991). The sun compass. Experientia Supplementum (Basel) 60, 1-15.
109. Schulten, K., Swenberg, C.E. & Weller, A. (1978). A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion. Zeitschrift fur Physical Chemistry NF111, 1-5.
110. Thorup, K. & Holland, R. (2009). The bird GPS. J. Exp. Biol. 212, 3597-3604.
111. Thorup, K. & Rabøl, J. (2001). The orientation system and migration pattern of long-distance migrants: conflict between model predictions and observed patterns. J. Avian Biol. 32, 111-119.
112. Thorup, K. & Rabøl, J. (2007). Compensatory behaviour following displacement in migratory birds. A meta-analysis of cage-experiments. Behav. Ecol. Sociobiol. 61, 825-841.
113. Thorup, K., Bisson, I., Bowlin, M., Holland, R.A., Ramenofsky, M., Wingfield, J. & Wikelski, M. (2007). Migration routes of adult and juvenile white-crowned sparrows differ after continent-wide displacement during migration. Proc. Nat. Acad. Sci. U.S.A. 104, 18115-18119.
114. Thorup, K., Holland, R.A., Tottrup, A.P. & Wikelski, M. (2010). Understanding the migratory orientation program of birds: extending laboratory studies to study free-flying migrants in a natural setting. Integr. Comp. Biol. 50, 315-322.
115. Thorup, K.T., Ortvad, T.E., Rabøl, J., Holland, R.A., Tøttrup, A.P. & Wikelski, M. (2011). Juvenile songbirds compensate for displacement of Oceanic Islands during autumn migration. PLoS ONE e6, 17903.
116. Treiber, C.D., Salzer, M.C., Riegler, J., Edelman, N., Sugar, C., Breuss, M., Pichler, P., Cadiou, H., Saunders, M., Lythgoe, M., Shaw, J. & Keays, D.A. (2012). Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484, 367-370.
117. Viguier, C. (1882). Le sens de l'orientation et ses organes chez les animaux et chez l'homme. Review Philisosophique Frances Etranger 14, 1-36.
118. Walcott, C. (1991). Magnetic maps in pigeons, In Orientation in birds: 38-51. Berthold, P. (Ed.). Basel: Birkhauser-Verlag.
119. Walcott, C. (1996). Pigeon homing: observations, experiments and confusions. J. Exp. Biol. 199, 21-27.
120. Walcott, C. & Michener, M.C. (1971). Sun navigation in homing pigeons-attempts to shift the sun's coordinates. J. Exp. Biol. 54, 291-316.
121. Waldvogel, J.A. & Phillips, J.B. (1991). Olfactory cues perceived at the home loft are not essential for the formation of a navigational map in pigeons. J. Exp. Biol. 155, 643-660.
122. Waldvogel, J.A., Phillips, J.B. & Brown, A.I. (1988). Changes in the short term deflector loft effect are linked to the sun compass of homing pigeons. Anim. Behav. 36, 150-158.
123. Walker, M.M. (1998). On a wing and a vector: a model for magnetic navigation in birds. J. Theor. Biol. 192, 341-349.
124. Wallraff, H.G. (1972). Homing of pigeons after extirpation of their cochleae and lagenae. Nat. New Biol. 236, 223-224.
125. Wallraff, H.G. (1974). Das Navigationssystem der Vögel. Munich: Oldenburg.
126. Wallraff, H.G. (1981). The olfactory component of pigeon navigation: steps and analysis. J. Comp. Physiol. 143, 411-422.
127. Wallraff, H.G. (1991). Conceptual approaches to avian navigation, In Orientation in Birds: 128-165. Berthold, P. (Ed.). Basel: Birkhauser.
128. Wallraff, H.G. (2005). Avian navigation: pigeon homing as a paradigm. Berlin: Springer.
129. Wallraff, H.G. & Andreae, M.O. (2000). Spatial gradients in ratios of atmospheric trace gasses: a study stimulated by experiments on bird navigation. Tellus 52B, 1138-1157.
130. Wallraff, H.G., Kiepenheuer, J., Neumann, M.F. & Streng, A. (1995). Homing experiments with starlings deprived of the sense of smell. Condor 97, 20-26.
131. Wikelski, M., Kays, R.W., Kasdin, N.J., Thorup, K., Smith, J.A. & Swenson, G.W. (2007). Going wild: what a global small-animal tracking system could do for experimental biologists. J. Exp. Biol. 210, 181-186.
132. Williams, N.M. & Wild, J.M. (2001). Trigeminally innervated iron-containing structures in the beak of homing pigeons, and other birds. Brain Res. 889, 243-246.
133. Wiltschko, R. (1996). The function of olfactory input in pigeon orientation: does it provide navigational information or play another role? J. Exp. Biol. 199, 113-119.
134. Wiltschko, R. & Wiltschko, W. (2003). Avian navigation: from historical to modern concepts. Anim. Behav. 65, 257-272.
135. Wiltschko, R. & Wiltschko, W. (2006). Magnetoreception. Bioessays 28, 157-168.
136. Wiltschko, R. & Wiltschko, W. (2013). The magnetite-based receptors in the beak of birds and their role in avian navigation. J. Comp. Physiol. A. Neuroethol Sens Neural Behav. Physiol. 199, 89-99.
137. Wiltschko, R., Schiffer, I., Fuhrmann, P. & Wiltschko, W. (2010). The role of magnetite based receptors in the beak in pigeon homing. Curr. Biol. 20, 1-5.
138. Wiltschko, W. & Wiltchko, R. (2007). Magnetoreception in birds: two receptors for two different tasks. J. Orn. 148, S61-S67.
139. Wiltschko, W. & Wiltschko, R. (1972). Magnetic compass of European robins. Science 176, 62-64.
140. Wiltschko, W. & 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.] 177, 363-369.
141. Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. (1993). Red light disrupts magnetic orientation of migratory birds. Nature 364, 525-527.
142. Wiltschko, W., Munro, U., Beason, R.C., Ford, H. & Wiltschko, R. (1994). A magnetic pulse leads to a temporary deflection in the orientation of migratory birds. Experientia 50, 697-700.
143. Wiltschko, W., Munro, U., Ford, H. & 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.
144. Wiltschko, W., Munro, U., Wiltschko, R. & Kirschvink, J.L. (2002a). Magnetite-based magnetoreception in birds: the effect of a biasing field and a pulse on migratory behavior. J. Exp. Biol. 205, 3031-3037.
145. Wiltschko, W., Traudt, J., Gunturkun, O., Prior, H. & Wiltschko, R. (2002b). Lateralisation of magnetic compass orientation in a migratory bird. Nature 419, 467-470.
146. Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. (2006). Bird navigation: what type of information does the magnetite-based receptor provide. Proc. R. Soc. Lond. B. 273, 2815-2820.
147. Wiltschko, W., Ford, H., Munro, U., Winklhofer, M. & Wiltschko, R. (2007). Magnetite-based magnetoreception: the effect of repeated pulsing on the orientation of migratory birds. J. Comp. Physiol. 193, 515-522.
148. Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. (2009). Avian orientation: the pulse effect is mediated by the magnetite receptors in the upper beak. Proc. R. Soc. Lond. B. 276, 2227-2232.
149. Wu, L.-Q. & Dickman, J.D. (2011). Magnetoreception in an avian brain in part mediated by inner ear lagena. Curr. Biol. 21, 418-423.
150. Wu, L.-Q. & Dickman, J.D. (2012). Neural correlates of a magnetic sense. Science 336, 1054-1057.
151. Yorke, E.D. (1979). A possible magnetic transducer in birds. J. Theor. Biol. 77, 101-105.
152. Zapka, M., Heyers, D., Hein, C.M., Engels, S., Schneider, N.-L., Hans, J., Weiler, S., Dreyer, D., Kishkinev, D., Wild, J.M. & Mouritsen, H. (2009). Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461, 1274-1277.