Advertisement

Journal of Comparative Physiology A

, Volume 204, Issue 8, pp 761–771 | Cite as

Only natural local odours allow homeward orientation in homing pigeons released at unfamiliar sites

  • Anna Gagliardo
  • Enrica Pollonara
  • Martin Wikelski
Original Paper

Abstract

According to the olfactory navigation hypothesis, birds are able to exploit the spatial distribution of environmental odourants to determine the direction of displacement and navigate from non-familiar locations. The so-called “olfactory activation hypothesis” challenged the specific role of olfactory cues in navigation by suggesting that olfactory stimuli only activate a navigational system that is based on non-olfactory cues, predicting that even artificial odourants alone are sufficient to allow unimpaired navigation. In this experiment, we compared tracks of experimental birds exposed to different olfactory stimuli before being made anosmic at the release site prior to release. One group of pigeons was exposed to purified air enriched with artificial odourants, while a second group was exposed to environmental air. The birds stimulated with artificial nonsense odourants displayed several behavioural differences from both untreated controls and anosmic pigeons exposed to environmental air prior to release: nonsense odourants birds were unable to determine the home direction, they mostly flew within a space outside the homeward oriented quadrant, and they flew shorter distances on the day of release. Our data failed to support a mere activational role of olfactory stimuli in navigation, and are consistent with the olfactory navigation hypothesis.

Keywords

Olfaction Homing pigeon Navigation GPS tracking Anosmia 

Notes

Acknowledgements

Our experiment has been conducted in accordance with the Italian law on animal welfare (Permit number 8630/2011). We are grateful to Tim Guilford for participating to the release performed on the 21st of August 2013. Fabio Chini and Andrea Guidi greatly helped in preparing and performing the experiment. Daniele Santerini helped in the figures preparation.

Supplementary material

359_2018_1277_MOESM1_ESM.pdf (1.2 mb)
Supplementary material 1 (PDF 1218 KB)

References

  1. Batschelet E (1981) Circular statistics in biology. Academic Press, LondonGoogle Scholar
  2. Bedini C, Fiaschi V, Lanfranchi A (1976) Olfactory nerve reconstitution in homing pigeon after resection—ultrastructural and electrophysiological data. Arch Ital Biol 114:1–22PubMedGoogle Scholar
  3. Benvenuti S, Wallraff HG (1985) Pigeon navigation: site simulation by means of atmospheric odours. J Comp Physiol A 156:737–746CrossRefGoogle Scholar
  4. Benvenuti S, Ioalè P, Gagliardo A, Bonadonna F (1992) Effects of zinc sulphate-induced anosmia of homing behaviour of pigeons. Comp Biochem Physiol A 103:519–526CrossRefGoogle Scholar
  5. Bingman VP, Mench JA (1990) Homing behavior of hippocampus and parahippocampus lesioned pigeons following short-distance releases. Behav Brain Res 40:227–238CrossRefPubMedGoogle Scholar
  6. Bingman VP, Bagnoli P, Ioalè P, Casini G (1984) Homing behavior of pigeons after telencephalic ablations. Brain Behav Evol 24:94–108CrossRefPubMedGoogle Scholar
  7. Bingman VP, Ioalè P, Casini G, Bagnoli P (1988) Hippocampal ablated homing pigeons show a persistent impairment in the time taken to return home. J Comp Physiol A 163:559–563CrossRefGoogle Scholar
  8. Bingman VP, Gagliardo A, Hough GE, Ioalè P, Kahan NC, Siegel JJ (2005) The avian hippocampus, homing in pigeons and the memory representation of large scale space. Integr Comp Biol 45:555–564CrossRefPubMedGoogle Scholar
  9. Cancalon P (1982) Degeneration and regeneration of olfactory cells induced by ZnSO4 and other chemicals. Tissue Cell 14:713–733CrossRefGoogle Scholar
  10. Gagliardo A (2013) Forty years of olfactory navigation in birds. J Exp Biol 216:2165–2171CrossRefPubMedGoogle Scholar
  11. Gagliardo A, Odetti F, Ioalè P (2001) Relevance of visual cues for orientation at familiar sites by homing pigeons: an experiment in a circular arena. Proc Roy Soc Lond B 268:1–6CrossRefGoogle Scholar
  12. Gagliardo A, Ioalè P, Savini M, Lipp H-P, Dell’Omo G (2007) Finding home: the final step of the pigeons’ homing process studied with a GPS data logger. J Exp Biol 210:1132–1138CrossRefPubMedGoogle Scholar
  13. Gagliardo A, Ioalè P, Filannino C, Wikelski M (2011) Homing pigeons only navigate with intact environmental odours: a test of the olfactory activation hypothesis with GPS data loggers. PlosOne 6:e22385CrossRefGoogle Scholar
  14. Gagliardo A, Bried J, Lambardi P, Luschi P, Wikelski M, Bonadonna F (2013) Oceanic navigation in Cory’s shearwaters: evidence for a crucial role of olfactory cues for homing after displacement. J Exp Biol 216:2798–2805CrossRefPubMedGoogle Scholar
  15. Gagliardo A, Pollonara E, Coppola VJ, Santos CD, Wikelski M, Bingman VP (2014) Evidence for perceptual neglect of environmental features in hippocampal-lesioned pigeons during homing. Eur J Neurosci 40:3102–3110CrossRefPubMedGoogle Scholar
  16. Gagliardo A, Pollonara E, Wikelski M (2016) Pigeon navigation: exposure to environmental odours prior to release is sufficient for homeward orientation, but not for homing. J Exp Biol 219:2475–2480CrossRefPubMedGoogle Scholar
  17. Guilford T, Gagliardo A, Chappell J, Bonadonna F, Burt de Pereira T, Holland R (1998) Homing pigeons use olfactory cues for navigation in England. J Exp Biol 201:895–900PubMedGoogle Scholar
  18. Holland RA, 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 212:4065–4071CrossRefPubMedGoogle Scholar
  19. Jorge PE, Marques AM, Phillips JB (2009) Activational rather than navigational effects of odors on homing of young pigeons. Curr Biol 19:650–654CrossRefPubMedGoogle Scholar
  20. Jorge PE, Marques AM, Phillips JB (2010) Activational effects of odours on avian navigation. Proc Roy Soc Lond B 277:45–49CrossRefGoogle Scholar
  21. Jorge PE, Phillips JB, Goncalves A, Marques AM, Nemec P (2014) Odours stimulate neuronal activity in the dorsolateral area of the hippocampal formation during path integration. Proc Roy Soc B 281:20140025CrossRefGoogle Scholar
  22. Padget O, Dell’Ariccia G, Gagliardo A, González-Solís J, Guilford T (2017) Anosmia impairs homing orientation but not foraging behaviour in free-ranging shearwaters. Sci Rep 7:9668CrossRefPubMedPubMedCentralGoogle Scholar
  23. Papi F (1986) Pigeon navigation: solved problems and open questions. Monit Zool Ital (N S) 20:471–517Google Scholar
  24. Papi F, Fiore L, Fiaschi V, Benvenuti S (1971) The influence of olfactory nerve section on the homing capacity of carrier pigeons. Monit Zool Ital (N S) 5:265–267Google Scholar
  25. Phillips JB, Jorge PE (2014) Olfactory navigation: failure to attempt replication of critical experiments keeps controversy alive. Reply to Wallraff Anim Behav 90:e7–e9CrossRefGoogle Scholar
  26. Pollonara E, Luschi P, Guilford T, Wikelski M, Bonadonna F, Gagliardo A (2015) Olfaction and topography, but not magnetic cues, control navigation in a pelagic seabird: displacements with shearwaters in the Mediterranean sea. Sci Rep 5:16486CrossRefPubMedPubMedCentralGoogle Scholar
  27. Wallraff HG (1966) Über die Heimfindeleistung von Brieftauben nach Haltung in verschiedenartig abgeschirmten Volieren. Z Vergl Physiol 52:215–259CrossRefGoogle Scholar
  28. Wallraff HG (2005) Avian navigation: pigeon homing as a paradigm. Springer, BerlinGoogle Scholar
  29. Wallraff HG (2014) Do olfactory stimuli provide positional information for home-oriented avian navigation? Anim Behav 90:e1–e6CrossRefGoogle Scholar
  30. Wallraff HG (2015) An amazing discovery: bird navigation based on olfaction. J Exp Biol 218:1464–1466CrossRefPubMedGoogle Scholar
  31. Wallraff HG, Foà A (1981) Pigeon navigation: charcoal filter removes relevant information from environmental air. Behav Ecol Sociobiol 9:67–77CrossRefGoogle Scholar
  32. Wallraff HG, Kiepenheuer J, Neumann MF, Sinsch U (1992) Microclimatic origin of inhaled air affects olfactory navigation of homing pigeons. Experientia 48:1153–1158CrossRefGoogle Scholar
  33. Wikelski M, Arriero E, Gagliardo A, Holland RA, Huttunen MJ, Juvaste R, Mueller I, Tertitski G, Thorup K, Wild M, Alanko M, Bairlein F, Cherenkov A, Cameron A, Flatz R, Hannila J, Hüppop O, Kangasniemi M, Kranstauber B, Penttinen M-L, Safi K, Semashko V, Schmid H, Wistbacka R (2015) True navigation in migrating gulls requires intact olfactory nerves. Sci Rep 5:17061CrossRefPubMedPubMedCentralGoogle Scholar
  34. Zar JH (1984) Biostatistical analysis. Prentice-Hall, Englewood CliffsGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Anna Gagliardo
    • 1
  • Enrica Pollonara
    • 1
  • Martin Wikelski
    • 2
  1. 1.Department of BiologyUniversity of PisaPisaItaly
  2. 2.Department for Migration and Immuno-ecologyMax Planck Institute for OrnithologyRadolfzellGermany

Personalised recommendations