Cues indicating location in pigeon navigation

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 201, Issue 10, 2015, Pages 961-967

  Beason, Robert C ^a   Wiltschko, Wolfgang ^b  

^a FB Biowissenschaften Goethe Universität Frankfurt ^*  (United States)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

Gravity; Infrasound; Magnetic field; Olfaction; Visual landmarks

Indexed keywords

ANIMAL; ASSOCIATION; GRAVITY; MAGNETIC FIELD; ODOR; ORIENTATION; PHYSIOLOGY; PIGEONS AND DOVES; SPATIAL ORIENTATION;

ANIMALS; COLUMBIDAE; CUES; GRAVITATION; MAGNETIC FIELDS; ODORS; ORIENTATION; SPATIAL NAVIGATION;

EID: 84941997882     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-015-1027-2     Document Type: Review

References (88)

1. Armstrong C, Wilkinson H, Meade J, Biro D, Freeman R, Guilford T (2013) Homing pigeons respond to the time-compensated solar cues even in sight of the loft. PLoS One 8:e63130
2. Arrowsmith SJ, Hedlin MAH (2005) Observations of infrasound from surf in southern California. Geophysical Res Lett 32:L09810
3. Beason RC, Semm P (1987) Magnetic responses of the trigeminal nerve system of the bobolink, Dolichonyx oryzivorus (Aves: Icteridae). Neurosci Lett 80:229–234
4. Beason RC, Semm P (1996) Does the avian ophthalmic nerve carry magnetic navigational information? J Exp Biol 199:1241–1244
5. Beason RC, Wiltschko R, Wiltschko W (1997) Pigeon homing: effects of magnetic pulses on initial orientation. Auk 114:405–415
6. Bedard AJ Jr, Georges TM (2000) Atmospheric infrasound. Phys Today 3:32–37
7. Benhamou S (2003) Bicoordinate navigation based on non-orthogonal gradient fields. J Theor Biol 224:235–239
8. Benvenuti S, Fiaschi (1983) Pigeon homing: combined effect of olfactory deprivation and visual impairment. Comp Biochem Physiol 76A:719–7251
9. Benvenuti S, Wallraff HG (1985) Pigeon navigation: site simulation by means of atmospheric odours. J Comp Physiol A 156:737–746
10. Biro D, Freeman R, Meade J, Roberts SJ, Guilford T (2007) Pigeons combine compass and landmark guidance in familiar route navigation. Proc Natl Acad Sci USA 104:7471–7476
11. Blaser N, Guskov SI, Meskenaile V, Kanevskyi VA, Lipp HP (2013) Altered orientation and flight path of pigeons reared on gravity anomalies: a GPS-tracking study. PLoS One 8:e77102
12. Blaser N, Guskov SI, Entin VA, Wolfer DP, Kanevskyi VA, Lipp HP (2014) Gravity anomalies without geomagnetic disturbances interfere with pigeon homing—a GPS tracking study. J Exp Biol 217:4057–4067
13. Chelazzi C, Pardi L (1972) Experiments on the homing behavior of caged pigeons. Monit Zool. Ital (NS) 6:11–16
14. Dennis TE, Rayner MJ, Walker MM (2007) Evidence that pigeons orient to geomagnetic intensity during homing. Proc R Soc B 274:1153–1158
15. Deutschlander ME, Beason RC (2014) Avian navigation and geographic positioning. J Field Ornithol 85:111–133
16. Deutschlander M, Phillips JB, Munro U (2012) Age-dependent orientation of magnetically-simulated geographic displacement in migratory Australian Silvereyes (Zosterops l. lateralis). Wilson J Ornithol 124:457–477
17. Dornfeld K (1991) Pigeon homing in relation to geomagnetic gravitational, topographical, and meteorological conditions. Behav Ecol Sociobiol 28:107–1123
18. 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 common features of birds. PLoS One 5:e9231
19. Fitzke FW, Hayes BP, Hodos W, Holden AL, Low CJ (1985) Refractive sectors in the visual field of the pigeon eye. J Physiol 369:17–31
20. Fleissner G, Stahl B, Thalau P, Falkenberg G, 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
21. Gagliardo A, Ioalè P, Fillannino C, Wikelski M (2011) Homing pigeons only navigate in air with intact environmental odours: a test of the olfactoy activation hypothesis with GPS data loggers. PLoS ONE 6:e22385
22. Griffin DR (1952) 1952. Bird navigation. Biol Rev Cambridge Phil Soc 27:359–400
23. Griffin DR, Hopkins CR (1976) Sounds audible to migrating birds. Anim Behav 22:672–678
24. Guilford T, Biro D (2014) Route following and the pigeon’s familiar area map. J Exp Biol 217:169–179
25. Hagstrum JT (2000) Infrasound and the avian navigational map. J Exp Biol 203:1103–1111
26. Hagstrum JT (2013) Atmospheric propagation modeling indicates homing pigeons use loft-specific infrasonic ‘map’ cues. J Exp Biol 216:687–699
27. Hagstrum JT, Manley GA (2015) Releases of surgically deafened homing pigeons indicate that aural cues play a significant role in their navigational system. J Comp Physiol A. doi:10.1007/s00359-015-1026-3
28. Henshaw I, Fransson T, Jakobsson Kuklberg (2010) Geomagnetic field affects spring migratory direction in a long distance migrant. Behav Ecol Sociobiol 64:1317–1323
29. Heyers D, Zaka M, Hoffmeister M, Wild JM, Mouritsen H (2010) Magnetic field changes activate the trigeminal brain stem complex in a migratory bird. Proc Natl Acad Sci USA 107:9394–9399
30. Hodos W, Erichson JT (1990) Lower-field myopia in birds: an adaptation that keeps the ground in focus. Vision Res 30:653–657
31. Holland RA (2003) The role of visual landmarks in the avian familiar area map. J Exp Biol 206:1773–1778
32. Holland RA (2014) True navigation in birds: from quantum physics to global migration. J Zool 293:1–15
33. Holland RA, 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
34. Jorge PE, Marques AE, Phillips JB (2009) Activational rather than navigational effects of odors of homing of young pigeons. Curr Biol 19:650–654
35. Jorge PE, Marques PAM, Phillips JB (2010) Activational effects of odours on avian navigation. J R Soc B 277:45–49
36. Jorge PE, Phillips JB, Gonçalves A, Marques PAM, Nĕmec P (2014) Odours stimulate neuronal activity in the dorsolateral area of the hippocampal formation during path integration. Proc R Soc B 281:20140025
37. Keeton WT (1973) Release-site bias as a possible guide to the “map”component in pigeons homing. J Comp Physiol 86:1–16
38. Keeton WT (1974) The orientational and navigational basis of homing in birds. Adv Stud Behav 8:47–132
39. Keeton WT, Brown AI (1976) Homing behavior of pigeons not disturbed by application of an olfactory stimulus. J Comp Physiol A 105:252–266
40. Keeton WT, Larkin TS, Windsor DM (1974) Normal fluctuations in the Earth’s magnetic field influence pigeon orientation. J Comp Physiol 95:95–103
41. Keeton WT, Kreithen ML, Hermayer KL (1977) Orientation of pigeons deprived of olfaction by nasal tubes. J Comp Physiol A 114:289–299
42. Kiepenheuer J (1982) The effect of magnetic anomalies on the homing behavior of pigeons. In: Wallraff HG (ed) Papi F. Avian navigation, Springer, pp 120–128
43. Kowalski U (1994) Das Richtungsverhalten verfrachteter Brietauben (Columba livia) im Orientierungskäfig. J Ornithol 135:17–35
44. Kramer G (1953) Wird die Sonnenhöhe bei der Heimfindeorientierung verwertet? J Ornithol 94:201–219
45. Kramer G (1957) Experiments in bird orientation and their interpretation. Ibis 99:196–227
46. Kramer G (1959) Recent experiments in bird orientation. Ibis 101:399–416
47. Kreithen ML, Eisner T (1978) Ultraviolet light detection by the homing pigeon. Nature 272:347–348
48. Kreithen ML, Quine DB (1979) Infrasound detection by the homing pigeon: a behavioral audiogram. J Comp Physiol A 129:1–4
49. Lednor AJ, Walcott C (1984) The orientation of pigeons at gravity anomalies. J Exp Biol 111:259–263
50. Lefeld N, Heyers D, Schneider NL, Engels S, Elbers D, Mouritsen H (2014) Magnetic field-driven induction of ZENK in the trigeminal system of pigeons (Columba livia). J R Soc Interface 11:2014077
51. Martin GR (2014) The subtlety of simple eyes: the tuning of visual fields to perceptual challenges in birds. Phil Trans R Soc B 369:20130040
52. Mazzotto M, Nacci L, Gagliardo A (1999) Homeward orientation of pigeons confined in a circular arena. Behav Processes 46:217–225
53. Mora CV, Davison M, Wild JM, Walker MM (2004) Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432:508–511
54. Mukhin A, Chernetsov N, KishkinevV DD (2008) Acoustic information as a distant cue for habitat recognition by nocturnally migrating passerines. Behav Ecol 19:716–723
55. Papi F (1986) Pigeon navigation: solved problems and open questions. Monit Zool Itali (NS) 20:471–517
56. Papi F (2001) Animal navigation at the end of the century: a retrospect and a look forward. Ital J Zool 68:171–180
57. Papi F, Fiore L, Fiaschi V, Benvenuto S (1972) Olfaction and homing in pigeons. Monit Zool Ital (NS) 6:85–95
58. Papi F, Keeton WT, Brown AI, Benvenuti S (1978a) Do American and Italian pigeons rely on different homing mechanisms? J Comp Physiol A 128:303–317
59. Papi F, Ioalé P, Fiaschi V, Benvenuti S, Baldaccini NE (1978b) Pigeon homing: cues detected during the outward journey influence initial orientation. In: Schmidt-Koenig K, Keeton WT (eds) Animal migration navigation and homing. Springer, Berlin, pp 63–77
60. Phillips JB, Jorge PE (2014) Olfactory navigation: failure to attempt replication of critical experiments keep controversy alive. Reply to Wallraff. Anim Behav 90:e7–e9
61. Quine DB, Kreithen ML (1981) Frequency shift discrimination: can homing pigeons locate infrasounds by Doppler shifts? J Comp Physiol A 141:153–155
62. Schermuly L, Klinke R (1990) Infrasound sensitive neurones in the pigeon cochlear ganglion. J Comp Physiol A 166:355–363
63. Schiffner I, Wiltschko R (2011) Temporal fluctuations of the geomagnetic field affect pigeons’ entire homing flight. J Comp Physiol A 197:765–772
64. Schiffner I, Fuhrmann P, Wiltschko R (2011) Tracking pigeons in a magnetic anomaly and in magnetically ‘quiet’ terrain. Naturwissenschaften 97:575–581
65. Schlichte HJ (1973) Untersuchungen über die Bedeutung optischer Parameter für das Heimkehrverhalten der Brieftauben. Z Tierpsychol 32:257–280
66. Schmidt-Koenig K, Walcott C (1978) Tracks of pigeons homing with frosted lenses. Anim Behav 26:480–486
67. Semm P, Beason RC (1990) Responses to small magnetic variations by the trigeminal system of the Bobolink. Brain Res Bull 25:735–740
68. Tian L, Xiao B, Lin W, Zhang S, Zhu R, Pan Y (2006) Testing the presence of magnetite in the upper-beak skin of homing pigeons. Biometals 20:197–203
69. Treiber CD, Salzer MC, Riegler J, Edelman N, Breuss M, Pichler P, Cadjou H, Saunders M, Lythgoe M, Shaw J, Keays DA (2012) Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484:367–370
70. Walcott C (1978) Anomalies in the Earth’s magnetic field increase the scatter in pigeons’ vanishing bearings. In: Schmidt-Koenig K, Keeton WT (eds) Animal migration, navigation and homing. Springer, Berlin, pp 143–151
71. Walcott C (1992) Pigeons at magnetic anomalies: the effect of loft location. J Exp Biol 170:127–141
72. Walcott C (2005) Multi-modal orientation cues in homing pigeons. Integr Comp Biol 45:574–581
73. Walcott C, Gould JL, Kirschvink JL (1979) Pigeons have magnets. Science 205:1027–1029
74. Wallraff HG (2004) Avian olfactory navigation: its empirical foundation and conceptual state. Anim Behav 67:189–204
75. Wallraff HG (2005a) Avian navigation: pigeon homing as a paradigm. Springer-Verlag, Heidelberg
76. Wallraff HG (2005b) Beyond familiar landmarks and integrated routes: goal-oriented navigation by birds. Conn Sci 17:91–106
77. Wallraff HG (2014) Do olfactory stimuli provide positional information for home-oriented avian navigation? Anim Behav 90:e1–e6
78. Wiltschko W, Wiltschko R (2007) Magnetoreception in birds: two receptors for two different tasks. J Ornithol 148(Suppl 1):S61–S76
79. Wiltschko R, Wiltschko W (2009) Avian navigation. Auk 126:717–743
80. Wiltschko R, Wiltschko W (2013) The magnetite-based receptors in the beak of birds and their role in avian navigation. J Comp Physiol A 199:89–98
81. Wiltschko R, Wiltschko W (2014) Sensing magnetic directions in birds: radical pair processes involving cryptochrome. Biosensors 4:221–242
82. Wiltschko R, Wiltschko W (2015) Avian navigation: a combination of innate and learned mechanisms. Adv Stud Behav 47:229–310
83. Wiltschko W, Wiltschko R, Foa A, Benvenuti S (1986) Orientation behaviour of pigeons deprived of olfactory information during the outward journey and at the release site. Monit Zool Ital (NS) 20:183–193
84. Wiltschko W, Wiltschko R, Walcott C (1987a) Pigeon homing: different effects of olfactory deprivation in different countries. Behav Ecol Sociobiol 21:333–342
85. Wiltschko W, Wiltschko R, Grüter M (1987b) Pigeon homing: early experience determines what factors are used for navigation. Naturwissenschaften 74:196–198
86. Wiltschko R, Stapput K, Siegmund B (2005) Navigational strategies at familiar sites. Behav Ecol Sociobiol 59:303–312
87. Wiltschko R, Schiffner I, Wiltschko W (2009a) A strong magnetic anomaly affects pigeon navigation. J Exp Biol 212:2983–2990
88. Wiltschko W, Munro U, Ford H, Wiltschko R (2009b) Avian orientation: the pulse effect is mediated by the magnetite receptors in the upper beak. Proc R Soc B 276:2227–2232