Mathematical analysis of the homing flights of pigeons based on GPS tracks

Abstract

To analyse the effect of magnetic and olfactory deprivation on the homing flight of pigeons, we released birds from a familiar site with either their upper beak or their nostrils anaesthetized. The tracks were analysed by time lag embedding to calculate the short-term correlation dimension, a variable that reflects the degrees of freedom and thus the number of factors involved in a system. We found that higher natural fluctuations in the earth’s magnetic field characterized by A P-indices of 8 and above caused a reduction of the correlation dimension of the control birds. We thus separated the data into two groups according to whether they were recorded on magnetically quiet days or on days with higher magnetic fluctuations. Anaesthetizing the upper beak had no significant effect. Making pigeons anosmic reduced the correlation dimension on magnetically quiet days, but did not cause any reduction on days with higher fluctuations. Altogether, our data suggest an involvement of magnetic cues and olfactory factors during the homing flight and point to a robust, multi-factorial map.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Beason RC, Wiltschko W (2015) Cues indicating location in pigeon navigation. J Comp Physiol A 201:961–967

    Article  Google Scholar 

  2. Beason RC, Wiltschko R, Wiltschko W (1997) Pigeon homing: effects of magnetic pulses on initial orientation. Auk 114:405–415

    Article  Google Scholar 

  3. Benvenuti S, Fiaschi V (1983) Pigeon homing: combined effect of olfactory deprivation and visual impairment. Comp Biochem Physiol 76A:719–725

    Article  Google Scholar 

  4. Chelazzi C, Pardi L (1972) Experiments on the homing behavior of caged pigeons. Monit Zool Ital 6:11–16

    Google Scholar 

  5. Dennis TE, Rayner MJ, Walker MM (2007) Evidence that pigeons orient to geomagnetic intensity during homing. Proc R Soc B 274:1153–1158

    Article  PubMed  PubMed Central  Google Scholar 

  6. Falkenberg G, Fleissner G, Schuchardt K, Kuehbacher M, Thalau P, Mouritsen H, Heyer 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Fleissner G, Holtkamp-Rötzler E, Hanzlik M, Winklhofer M, Fleissner G, Petersen N, Wiltschko W (2003) Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J Comp Neurol 458:350–360

    CAS  Article  PubMed  Google Scholar 

  8. Gagliardo A (2013) Forty years of olfactory navigation in birds. J Exp Biol 216:2165–2171

    Article  PubMed  Google Scholar 

  9. Gagliardo A, Ioalè 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-loggers. PLoS ONE 6:e22385

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 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 219:2475–2480

    Article  PubMed  Google Scholar 

  11. Grassberger P, Procaccia I (1983) Characterization of strange attractors. Phys Rev Lett 50:346–349

    Article  Google Scholar 

  12. Hitchcock HB (1952) Airplane observations of homing pigeons. Proc Am Philos Soc 96:270–289

    Google Scholar 

  13. Holland R, Filannino C, Gagliardo A (2013) A magnetic pulse does not affect homing pigeon navigation: a GPS tracking experiments. J Exp Biol 216:2192–2200

    Article  PubMed  Google Scholar 

  14. Jandacka P, Burda H, Pistora J (2014) Magnetically induced behavior of ferritin corpuscles in avian ears: can cuticulosomes function as magnetosomes? J R Soc Interface 12:20141087

    Article  CAS  Google Scholar 

  15. Jorge PE, Marques AE, Phillips JB (2009) Activational rather than navigational effects of odors on young pigeon homing. Curr Biol 19:650–654

    CAS  Article  PubMed  Google Scholar 

  16. Jorge PE, Marques AE, Phillips JB (2010) Activational effects of odours on avian navigation. Proc R Soc B 277:45–49

    Article  PubMed  Google Scholar 

  17. Jorge PE, Phillips JN, Goncalves A, Marques PAM, Nemec P (2014) Odours stimulate neuronal activity in the dorsolateral area of the hippocampal formation during path integration. Proc R Soc B 281:20140025

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Keeton WT (1974) The orientational and navigational basis of homing in birds. Adv Study Behav 5:47–132

    Article  Google Scholar 

  19. Keeton WT, Larkin TS, Windsor DM (1974) Normal fluctuations in the earth’s magnetic field influence pigeon orientation. J Comp Physiol 95:95–103

    Article  Google Scholar 

  20. Kiepenheuer J (1982) The effect of magnetic anomalies on the homing behaviour of pigeons. In: Papi F, Wallraff HG (eds) Avian navigation. Springer, Berlin, pp 120–128

    Google Scholar 

  21. Kowalski U (1974) Das Richtungsverhalten verfrachteter Brietauben (Columba livia) im Orientierungskäfig. J Ornithol 135:17–35

    Article  Google Scholar 

  22. Kowalski U, Wiltschko R, Füller E (1988) Normal fluctuations of the geomagnetic field may affect initial orientation in pigeons. J Comp Physiol 163:593–600

    Article  Google Scholar 

  23. Kramer G (1953) Wird die Sonnenhöhe bei der Heimfindeorientierung verwertet? J Ornithol 94:201–219

    Article  Google Scholar 

  24. Kramer G (1957) Experiments in bird orientation and their interpretation. Ibis 99:196–227

    Article  Google Scholar 

  25. Lauwers M, Pichler P, Edelmann NB, Resch GP, Ushakova L, Salzer MC, Heyers D, Saunders M, Shaw J, Keays DA (2013) An iron-rich organelle in the cuticular plate of avian hair cells. Curr Biol 23:924–929

    CAS  Article  PubMed  Google Scholar 

  26. Lincoln JV (1967) Geomagnetic indices. In: Matsushita S, Cambell HW (eds) Physics of geomagnetic phenomena. Academic Press, London, pp 67–100

    Google Scholar 

  27. Mazzotto M, Nacci L, Gagliardo A (1999) Homeward orientation of pigeons confined in a circular arena. Behav Proc 46:217–225

    CAS  Article  Google Scholar 

  28. Michener MC, Walcott C (1967) Homing of single pigeons—analysis of tracks. J Exp Biol 47:99–131

    CAS  PubMed  Google Scholar 

  29. Papi F (1986) Pigeon navigation: solved problems and open questions. Monit Zool Ital 20:471–517

    Google Scholar 

  30. 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 5:265–267

    Google Scholar 

  31. Qin S, Yin H, Yang C, Dou Y, Liu Z, Zhang P, Yu H, Huang Y, Feng J, Hao J, Deng L, Yan X, Dong X, Zhao Z, Jiang T, Wang HW, Luo SJ, Xie C (2015) A magnetic protein biocompass. Nat Mater. doi:10.1038/NMAT4484

    PubMed  Google Scholar 

  32. Schiffner I, Wiltschko R (2009) Point of decision: when do pigeons decide to head home? Naturwissenschaften 96:251–258

    CAS  Article  PubMed  Google Scholar 

  33. Schiffner I, Wiltschko R (2011) Temporal fluctuations of the geomagnetic field affect pigeons’ entire flight. J Comp Physiol A 197:765–772

    Article  Google Scholar 

  34. Schiffner I, Wiltschko R (2013) Development of the navigational system in homing pigeons: increase in complexity of the navigational map. J Exp Biol 216:2675–2681

    Article  PubMed  Google Scholar 

  35. Schiffner I, Wiltschko R (2014) Pigeon navigation: different routes lead to Frankfurt. PLoS ONE 9:e112439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Schiffner I, Baumeister J, Wiltschko R (2011a) Mathematical analysis of the navigational process in homing pigeons. J Theor Biol 291:42–46

    Article  PubMed  Google Scholar 

  37. Schiffner I, Fuhrmann P, Wiltschko R (2011b) Tracking pigeons in a magnetic anomaly and in magnetically “quiet” terrain. Naturwissenschaften 98:575–581

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Schiffner I, Fuhrmann P, Wiltschko R (2013) Homing flights of pigeons in the Frankfurt region: the effect of distance and local experience. Anim Behav 86:291–307

    Article  Google Scholar 

  39. Schiffner I, Siegmund B, Wiltschko R (2014) Following the sun: a mathematical analysis of the tracks of clock-shifted homing pigeons. J Exp Biol 217:2643–2649

    Article  PubMed  Google Scholar 

  40. Skinner JE (1994) Low-dimensional chaos in biological systems. Nat Biotechnol 12:596–600

    CAS  Article  Google Scholar 

  41. Steiner I, Burgi C, Werffeli S, Dell’Omo G, Valenti P, Tröster G, Wolfe DP, Lipp HP (2000) A GPS logger and software for analysis of homing pigeons and small mammals. Physiol Behav 71:1–8

    Article  Google Scholar 

  42. Takens F (1981) Detecting strange attractors in turbulence. In: Rand D, Young LS (eds) Dynamical systems and turbulence, vol 898., lecture notes in mathematicsSpringer, Berlin, pp 366–381

    Google Scholar 

  43. Treiber CD, Salzer MC, Riegler J, Edelmann N, Sugar C, Breuss M, Pichler P, Cadiou H, Saunders 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

    CAS  PubMed  Google Scholar 

  44. von Hünerbein K, Hamann HJ, Rüter E, Wiltschko W (2000) A GPS-based system for recording the flight paths of birds. Naturwissenschaften 87:278–279

    Article  Google Scholar 

  45. Wagner G (1970) Verfolgung von Brieftauben im Helikopter. Rev Suisse Zool 77:39–60

    Article  Google Scholar 

  46. Walcott C (1978) Anomalies in the earth’s magnetic field increase the scatter of pigeons’ vanishing bearings. In: Schmidt-Koenig K, Keeton WT (eds) Animal migration, navigation, and homing. Springer, Berlin, pp 143–151

    Google Scholar 

  47. Walcott C (2005) Multi-modal orientation cues in homing pigeons. Integr Comp Biol 45:574–581

    Article  PubMed  Google Scholar 

  48. Wallraff HG (2004) Avian olfactory navigation: its empirical foundation and conceptual state. Anim Behav 67:189–204

    Article  Google Scholar 

  49. 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

    CAS  Article  Google Scholar 

  50. Wiltschko R, Wiltschko W (2014) Sensing magnetic directions in birds: radical pair processes involving cryptochrome. Biosensors 4:221–242

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. Wiltschko R, Wiltschko W (2015) Avian navigation: a combination of innate and learned mechanisms. Adv Study Behav 47:229–310

    Article  Google Scholar 

  52. Wiltschko R, Schiffner I, Siegmund B (2007) Homing flights of pigeons over familiar terrain. Anim Behav 74:1229–1240

    Article  Google Scholar 

  53. Wiltschko R, Schiffner I, Wiltschko W (2009) A strong magnetic anomaly affects pigeon navigation. J Exp Biol 212:2983–2990

    Article  PubMed  Google Scholar 

  54. Wiltschko R, Schiffner I, Fuhrmann P, Wiltschko W (2010) The role of the magnetite-based receptors in the beak in pigeon homing. Curr Biol 20:1534–1538

    CAS  Article  PubMed  Google Scholar 

  55. Wu LQ, Dickman JD (2011) Magnetoreception in an avian brain in part mediated by inner ear lagena. Curr Biol 21:418–423

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. Wu LQ, Dickman JD (2012) Neural correlates of a magnetic sense. Science 336:1054–1057

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

The Ap-indices were provided by the National Oceanic and Atmospheric Administration (Boulder, Colorado). The experiments were performed in accordance with the rules and regulations of animal welfare in Germany.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ingo Schiffner.

Ethics declarations

Conflict of interest

The authors declare no competing financial interests.

Funding

Our work was supported by the Deutsche Forschungsgemeinschaft (WI 988/7-2, grant to R.W).

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 31 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Schiffner, I., Denzau, S., Gehring, D. et al. Mathematical analysis of the homing flights of pigeons based on GPS tracks. J Comp Physiol A 202, 869–877 (2016). https://doi.org/10.1007/s00359-016-1127-7

Download citation

Keywords

  • Homing pigeons
  • Magnetic navigation
  • Olfactory input
  • Correlation dimension
  • GPS tracks