Forty years of olfactory navigation in birds

Journal of Experimental Biology

Volumn 216, Issue 12, 2013, Pages 2165-2171

  Gagliardo, Anna ^a  

^a UNIVERSITY OF PISA   (Italy)

Author keywords

Avian; Navigation; Olfaction

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ASSOCIATION; BIRD; ENVIRONMENT; NAVIGATION; ODOR; ORIENTATION; PHYSIOLOGY; PIGEONS AND DOVES; REVIEW; SMELLING;

AVIAN; NAVIGATION; OLFACTION;

ANIMALS; BIRDS; COLUMBIDAE; CUES; ENVIRONMENT; HOMING BEHAVIOR; ODORS; OLFACTORY PERCEPTION; ORIENTATION;

AVES; COLUMBA;

EID: 84878544036     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.070250     Document Type: Review

References (59)

1. Baldaccini, N. E., Benvenuti, S., Fiaschi, V. and Papi, F. (1975). Pigeon navigation: effects of wind deflection at home cage on homing behaviour. J. Comp. Physiol. 99, 177-186.
2. Benvenuti, S. and Gagliardo, A. (1996). Homing behaviour of pigeons subjected to unilateral zinc sulphate treatment of their olfactory mucosa. J. Exp. Biol. 199, 2531-2535.
3. Benvenuti, S. and Ranvaud, R. D. (2004). Olfaction and the homing ability of pigeons raised in a tropical area in Brazil. J. Exp. Zool. A Comp. Exp. Biol. 301, 961-967.
4. Benvenuti, S. and Wallraff, H. G. (1985). Pigeon navigation: site simulation by means of atmospheric odours. J. Comp. Physiol. A 156, 737-746.
5. 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.
6. Benvenuti, S., Fiaschi, V. and Foà, A. (1977). Homing behaviour of pigeons disturbed by application of an olfactory stimulus. J. Comp. Physiol. A 120, 173-179.
7. Benvenuti, S., Bingman, V. P. and Gagliardo, A. (1998). Effect of zinc-sulphate induced anosmia on pigeon homing: a comparison among birds in different regions. Trends Comp. Biochem. Physiol. 5, 221-228.
8. Bingman, V. P., Bagnoli, P., Ioalè, P. and Casini, G. (1984). Homing behavior of pigeons after telencephalic ablations. Brain Behav. Evol. 24, 94-108.
9. Biro, D., Meade, J. and Guilford, T. (2004). Familiar route loyalty implies visual pilotage in the homing pigeon. Proc. Natl. Acad. Sci. USA 101, 17440-17443.
10. Bonadonna, F., Benhamou, S. and Jouventin, P. (2003). Orientation in 'featureless' environments: the extreme case of pelagic birds. In Avian Migration (ed. P. Berthold, E. Gwinner and E. Sonnenschein), pp. 367-377. Berlin/Heidelberg: Springer.
11. 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.
12. Dell'Ariccia, G. and Bonadonna, F. (2013). Back home at night or out until morning? Nycthemeral variations in homing of anosmic Cory's shearwaters in a diurnal colony. J. Exp. Biol. 216, 1430-1433.
13. 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.
14. Fiaschi, V., Farina, M., and Ioalé, P. (1974). Homing experiments on swifts Apus apus (L.) deprived of olfactory perception. Monit. Zool. Ital. (N.S.) 8, 235-244.
15. Foà, A., Benvenuti, S., Ioalè, P. and Wallraff, H. G. (1984). Geographical and temporal variability in pigeon homing. Parallel studies in Italy and Germany. Behav. Ecol. Sociobiol. 15, 25-34.
16. Gagliardo, A., Mazzotto, M. and Bingman, V. P. (1997). Piriform cortex ablations block navigational map learning in homing pigeons. Behav. Brain Res. 86, 143-148.
17. Gagliardo, A., El Agbani, A. and Bingman, V. P. (2000). Olfaction and the navigational performance of homing pigeons on the Atlantic coast of Morocco. Ital. J. Zool. 67, 359-364.
18. Gagliardo, A., Ioalè, P., Odetti, F. and Bingman, V. P. (2001a). The ontogeny of the homing pigeon navigational map: evidence for a sensitive learning period. Proc. Biol. Sci. 268, 197-202.
19. Gagliardo, A., Odetti, F. and Ioalè, P. (2001b). Relevance of visual cues for orientation at familiar sites by homing pigeons: an experiment in a circular arena. Proc. Biol. Sci. 268, 2065-2070.
20. 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.
21. Gagliardo, A., Ioalè, P., Savini, M., Lipp, H.-P. and Dell'Omo, G. (2007). Finding home: the final step of the pigeons' homing process studied with a GPS data logger. J. Exp. Biol. 210, 1132-1138.
22. 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.
23. 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.
24. 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.
25. Guilford, T., Åkesson, S., Gagliardo, A., Holland, R. A., Mouritsen, H., Muheim, R., Wiltschko, R., Wiltschko, W. and Bingman, V. P. (2011). Migratory navigation in birds: new opportunities in an era of fast-developing tracking technology. J. Exp. Biol. 214, 3705-3712.
26. Holland, R. A. (2003). The role of visual landmarks in the avian familiar area map. J. Exp. Biol. 206, 1773-1778.
27. 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.
28. Hzn, J., Coemans, M. and Nuboer, J. (1995). No evidence for polarization sensitivity in the pigeon electroretinogram. J. Exp. Biol. 198, 325-335.
29. Ioalé, P. (1980). Further investigationson the homing behaviour of pigeons subjected to reverse wind direction at the loft. Monit. Zool. Ital. 14, 77-87.
30. Ioalè, P., Papi, F., Fiaschi, V. and Baldaccini, N. E. (1978). Pigeon navigation: effects upon homing behaviour by reversing wind direction at the loft. J. Comp. Physiol. 128, 285-295.
31. Ioalè, P., Nozzolini, M. and Papi, F. (1990). Homing pigeons do extract directional information from olfactory stimuli. Behav. Ecol. Sociobiol. 26, 301-305.
32. Jacobs, L. F. (2012). From chemotaxis to the cognitive map: the function of olfaction. Proc. Natl. Acad. Sci. USA 109 Suppl. 1, 10693-10700.
33. Jorge, P. E., Marques, P. A. and Phillips, J. B. (2010). Activational effects of odours on avian navigation. Proc. Biol. Sci. 277, 45-49.
34. Kramer, G. (1953). Wird die Sonnenhöhe bei der Heimfindeorientierung verwertet? J. Ornithol. 94, 201-219.
35. 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.
36. Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B. and Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853-858.
37. Nevitt, G. A. (2008). Sensory ecology on the high seas: the odor world of the procellariiform seabirds. J. Exp. Biol. 211, 1706-1713.
38. Papi, F. and Casini, G. (1990). Pigeons with ablated pyriform cortex home from familiar but not from unfamiliar sites. Proc. Natl. Acad. Sci. USA 87, 3783-3787.
39. Papi, F., Fiore, L., Fiaschi, V., and Benvenuti, S. (1971). The influence of olfactory nerve section on the homing capacity of carrier pigeons. Monit. Zool. Ital. 5, 265-267.
40. Papi, F., Fiore, L., Fiaschi, V. and Benvenuti, S. (1972). Olfaction and homing in pigeons. Monit. Zool. Ital. 6, 85-95.
41. Papi, F., Fiaschi, V., Benvenuti, S., and Baldaccini, N. E. (1973). Pigeon homing: outward journey detours influence the initial orientation. Monit. Zool. Ital. 7, 129-133.
42. Papi, F., Ioalè, P., Fiaschi, V., Benvenuti, S. and Baldaccini, N. E. (1974). Olfactory navigation of pigeons: the effect of treatment with odorous air currents. J. Comp. Physiol. A 94, 187-193.
43. Papi, F., Gagliardo, A., Fiaschi, V. and Dall'Antonia, P. (1989). Pigeon homing: does early experience determine what cues are used to navigate? Ethology 82, 208-215.
44. Patzke, N., Manns, M., Güntürkün, O., Ioalè, P. and Gagliardo, A. (2010). Navigation-induced ZENK expression in the olfactory system of pigeons (Columba livia). Eur. J. Neurosci. 31, 2062-2072.
45. Perdeck, A. C. (1958). Two types of orientation in migrating starlings, Sturnus vulgaris L., and chaffinches, Fringilla coelebs L., as revealed by displacement experiments. Ardea 46, 1-37.
46. Phillips, J. B. and Waldvogel, J. A. (1982). Reflected light cues generate the short-term deflector loft effect. In Avian Navigation (ed. F. Papi and H. G. Wallraff), pp. 190-202. Berlin: Springer-Verlag.
47. 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.
48. Walcott, C. (1991). Magnetic map in pigeons. In Orientation in Birds (ed. P. Berthold), pp. 38-51. Basel: Birkhäuser Verlag.
49. Walcott, C. (1996). Pigeon homing: observations, experiments and confusions. J. Exp. Biol. 199, 21-27.
50. Waldvogel, J. A. (1987). Olfactory navigation in homing pigeons: are the current models athmospherically realistic? Auk 104, 369-379.
51. Wallraff, H. G. (1970). Weitere Volierenversuche mit Brieftauben: wahrscheinlicher Einfluss dynamischer Faktorender Atmosphare auf die Orientierung. Z. Vgl. Physiol. 68, 182-201.
52. Wallraff, H. G. (1972). Homing of pigeons after extirpation of their cochleae and lagenae. Nat. New Biol. 236, 223-224.
53. Wallraff, H. G. (2000). Simulated navigation based on observed gradients of atmospheric trace gases (Models on pigeon homing, Part 3). J. Theor. Biol. 205, 133-145.
54. Wallraff, H. G. (2005a). Avian Navigation: Pigeon Homing as a Paradigm. Heidelberg: Springer-Verlag.
55. Wallraff, H. G. (2005b). Beyond familiar landmarks and integrated routes: goal-oriented navigation by birds. Connect. Sci. 17, 91-106.
56. Wallraff, H. G. and Andreae, M. O. (2000). Spatial gradients in ratios of atmospheric trace gases: a study stimulated by experiments on bird navigation. Tellus B Chem. Phys. Meteorol. 52, 1138-1157.
57. Wallraff, H. G. and Foà, A. (1981). Pigeon navigation: charcoal filter removes relevant information from environmental air. Behav. Ecol. Sociobiol. 9, 67-77.
58. 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.
59. Wiltschko, W. and Wiltschko, R. (1996). Magnetic orientation in birds. J. Exp. Biol. 199, 29-38.