Advertisement

Journal of Comparative Physiology A

, Volume 200, Issue 5, pp 399–407 | Cite as

Orientation of migratory birds under ultraviolet light

  • Roswitha WiltschkoEmail author
  • Ursula Munro
  • Hugh Ford
  • Katrin Stapput
  • Peter Thalau
  • Wolfgang Wiltschko
Original Paper

Abstract

In view of the finding that cryptochrome 1a, the putative receptor molecule for the avian magnetic compass, is restricted to the ultraviolet single cones in European Robins, we studied the orientation behaviour of robins and Australian Silvereyes under monochromatic ultraviolet (UV) light. At low intensity UV light of 0.3 mW/m2, birds showed normal migratory orientation by their inclination compass, with the directional information originating in radical pair processes in the eye. At 2.8 mW/m2, robins showed an axial preference in the east–west axis, whereas silvereyes preferred an easterly direction. At 5.7 mW/m2, robins changed direction to a north–south axis. When UV light was combined with yellow light, robins showed easterly ‘fixed direction’ responses, which changed to disorientation when their upper beak was locally anaesthetised with xylocaine, indicating that they were controlled by the magnetite-based receptors in the beak. Orientation under UV light thus appears to be similar to that observed under blue, turquoise and green light, albeit the UV responses occur at lower light levels, probably because of the greater light sensitivity of the UV cones. The orientation under UV light and green light suggests that at least at the level of the retina, magnetoreception and vision are largely independent of each other.

Keywords

Magnetoreception UV cones Monochromatic light Migratory orientation ‘Fixed direction’ responses 

Notes

Acknowledgments

Our work was supported by the Deutsche Forschungsgemeinschaft (grants to WW and RW). We sincerely thank H.J. Bischof, Universität Bielefeld, and L. Peichl, Max-Planck-Institute for Brain Research, Frankfurt am Main, for valuable discussions and comments, F. Geiser, University of New England, Armidale, for his logistic help and all students who participated in conducting the experiments, in particular S. Denzau and D. Gehring.

Ethical statement

The animal care and the performance of the experiments were in agreements with the laws, rules and regulations for animal welfare in Australia and Germany.

Supplementary material

359_2014_898_MOESM1_ESM.pdf (43 kb)
Supplementary material 1 (PDF 43 kb)

References

  1. Bailey MJ, Chong NW, Xiong J, Cassone VM (2002) Chickens’ Cry2: molecular analysis of an avian cryptochrome in retinal and pineal photoreceptors. FEBS Lett 513:169–174PubMedCrossRefGoogle Scholar
  2. Batschelet E (1981) Circular statistics in biology. Academic Press, LondonGoogle Scholar
  3. Bischof HJ, Nießner C, Peichl L, Wiltschko R, Wiltschko W (2011) Avian UV/violet cones as magnetoreceptors: the problem of separating visual and magnetic information. Commun Integr Biol 4:713–716PubMedCentralPubMedGoogle Scholar
  4. Cuthill IC, Partridge JC, Bennett AZD, Church SC, Hart NS, Hunt S (2000) Ultraviolet vision in birds. Adv Study Behav 29:159–214CrossRefGoogle Scholar
  5. Emlen ST, Emlen JT (1966) A technique for recording migratory orientation of captive bird. Auk 83:361–367CrossRefGoogle Scholar
  6. 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:e9231PubMedCentralPubMedCrossRefGoogle Scholar
  7. Fleissner G, Holtkamp-Rötzler E, Hanzlik M, Winklhofer M, Fleissner G, Petersen N, Wiltschko W (2003) Ultra-structural analysis of a putative magnetoreceptor in the beak of homing pigeons. J Comp Neurol 458:350–360PubMedCrossRefGoogle Scholar
  8. Goldsmith TH, Butler BK (2003) The roles of the receptor noise and cone oil droplets in the photopic spectral sensitivity of the budgerigar, Melopsittacus undulatus. J Comp Physiol A 189:135–142Google Scholar
  9. Haque R, Chaurasia SS, Wesse JH, Iovome PM (2002) Dual regulation of cryptochrome 1 mRNA expression in chicken retina by light and circadian oscillators. NeuroReport 13:2247–2251PubMedCrossRefGoogle Scholar
  10. Henbest KB, Kukura P, Rodger CT, Hore PJ, Timmel CR (2004) Radio frequency field effects on radical recombination reaction: a diagnostic test for the radical pair mechanism. J Am Chem Soc 126:8102–8103PubMedCrossRefGoogle Scholar
  11. Heyers D, Manns M, Luksch H, Güntürkün O, Mouritsen H (2007) A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLoS One 9:e937CrossRefGoogle Scholar
  12. Hunt DM, Peichl L (2013) S cones: evolution, retinal distribution, development, and spectral sensitivity. Vis Neurosci (in press). (http://dx.doi.org/10.1017/S0952523813000242)
  13. Keary N, Ruploh T, Voss J, Thalau P, Wiltschko R, Wiltschko W, Bischof HJ (2009) Oscillating magnetic field disrupts magnetic orientation in Zebra finches, Taeniopygia guttata. Front Zool 6:25PubMedCentralPubMedCrossRefGoogle Scholar
  14. Liedvogel M, Mouritsen H (2010) Cryptochromes—a potential magnetoreceptor: what do we know and what do we want to know? J R Soc Interface 7 suppl 2:147–162CrossRefGoogle Scholar
  15. Maier EJ (1992) Spectral sensitivities including the ultraviolet of the passeriform bird Leiothrix lutea. J Comp Physiol A 170:709–714CrossRefGoogle Scholar
  16. Möller A, Sagasser S, Wiltschko W, Schierwater B (2004) Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass. Naturwissenschaften 91:585–588PubMedCrossRefGoogle Scholar
  17. Nießner C, Denzau S, Gross J, Peichl L, Bischof HJ, Fleissner G, Wiltschko W, Wiltschko R (2011) Avian ultraviolet/violet cones identified as probable magnetoreceptors. PLoS One 6(5):20091CrossRefGoogle Scholar
  18. Nießner C, Denzau S, Stapput K, Ahmad M, Peichl L, Wiltschko W, Wiltschko R (2013) Magnetoreception: activated cryptochrome 1a concurs with magnetic orientation in birds. J R Soc Interface 10:20130630CrossRefGoogle Scholar
  19. Ritz T (2001) Disrupting magnetic compass orientation with a radio frequency oscillating field. In: Orientation and navigation—birds, humans and other animals. Royal Institute of Navigation, Oxford, paper 4Google Scholar
  20. Ritz T, Adem S, Schulten K (2000) A model for photoreceptor-based magnetoreception in birds. Biophys J 78:707–718PubMedCentralPubMedCrossRefGoogle Scholar
  21. Ritz T, Thalau P, Philllips JB, Wiltschko R, Wiltschko W (2004) Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429:177–180PubMedCrossRefGoogle Scholar
  22. Ritz T, Wiltschko R, Hore PJ, Rodgers CT, Stapput K, Thalau P, Timmel CR, Wiltschko W (2009) Magnetic compass of birds is based on a molecule with optimal directional sensitivity. Biophys J 96:3451–3457PubMedCentralPubMedCrossRefGoogle Scholar
  23. Semm P, Demaine C (1986) Neurophysiological properties of magnetic cells in the pigeon’s visual system. J Comp Physiol 159:619–625CrossRefGoogle Scholar
  24. Semm P, Nohr D, Demaine C, Wiltschko W (1984) Neural basis of the magnetic compass: interactions of visual, magnetic and vestibular inputs in the pigeon’s brain. J Comp Physiol 155:283–288CrossRefGoogle Scholar
  25. Stapput K, Güntürkün O, Hoffmann KP, Wiltschko R, Wiltschko W (2010) Magnetoreception of directional information in birds requires nondegraded vision. Curr Biol 20:259–1262CrossRefGoogle Scholar
  26. Thalau P, Ritz T, Stapput K, Wiltschko R, Wiltschko W (2005) Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften 92:86–90PubMedCrossRefGoogle Scholar
  27. Watari R, Yamaguchi C, Zemba W, Kubo Y, Okano K, Okano T (2012) Light-dependent structural change of chicken retinal cryptochrome4. J Biol Chem 287:42634–42641PubMedCentralPubMedCrossRefGoogle Scholar
  28. Wiltschko W, Wiltschko R, Munro U (2000) Light-dependent magnetoreception in birds: the effect of intensity of 565 nm green light. Naturwissenschaften 87:366–369PubMedCrossRefGoogle Scholar
  29. Wiltschko W, Traudt J, Güntürkün O, Prior H, Wiltschko R (2002) Lateralisation of magnetic compass orientation in a migratory birds. Nature 419:467–470PubMedCrossRefGoogle Scholar
  30. Wiltschko W, Munro U, Ford H, Wiltschko R (2003a) Lateralisation of magnetic compass orientation in Silvereyes, Zosterops lateralis. Aust J Zool 51:597–602CrossRefGoogle Scholar
  31. Wiltschko W, Munro U, Ford H, Wiltschko R (2003b) Magnetic orientation in birds: non-compass responses under monochromatic light of increased intensity. Proc R Soc Lond B 270:2133–2140CrossRefGoogle Scholar
  32. Wiltschko R, Ritz T, Stapput K, Thalau P, Wiltschko W (2005) Two different light-dependent responses to magnetic fields in birds. Curr Biol 16:1516–1523Google Scholar
  33. Wiltschko R, Stapput K, Bischof HJ, Wiltschko W (2007) Light-dependent magnetoreception in birds: increasing intensity of monochromatic light changes the nature of the response. Front Zool 4:5PubMedCentralPubMedCrossRefGoogle Scholar
  34. Wiltschko W, Freire R, Munro U, Ritz T, Rogers L, Thalau P, Wiltschko R (2007) The magnetic compass of domestic chickens, Gallus gallus. J Exp Biol 210:2300–2310PubMedCrossRefGoogle Scholar
  35. Wiltschko R, Munro U, Ford H, Stapput K, Wiltschko W (2008) Light-dependent magnetoreception: orientation behaviour of migratory birds under dim red light. J Exp Biol 211:3344–3350PubMedCrossRefGoogle Scholar
  36. Wiltschko R, Stapput K, Thalau P, Wiltschko W (2010) Directional orientation of birds by the magnetic field under different light conditions. J R Soc Interface 7 suppl 2:S163–S177PubMedCrossRefGoogle Scholar
  37. Wiltschko R, Dehe L, Gehring D, Thalau P, Wiltschko W (2013) Interaction between the visual and the magnetoreception system: different effects of bichromatic light regimes on the directional behavior of migratory birds. J Physiol (Paris) 107:137–146CrossRefGoogle Scholar
  38. Zapka M, Heyers D, Hein CM, Engels S, Schneider NL, Hans J, Weiler S, Dreyer D, Kishkinev D, Wild JM, Mouritsen H (2009) Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461:1274–1277PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Roswitha Wiltschko
    • 1
    Email author
  • Ursula Munro
    • 2
  • Hugh Ford
    • 3
  • Katrin Stapput
    • 1
  • Peter Thalau
    • 1
  • Wolfgang Wiltschko
    • 1
  1. 1.Fachbereich Biowissenschaften derJ.W.Goethe-Universität FrankfurtFrankfurt am MainGermany
  2. 2.School of the EnvironmentUniversity of Technology, SydneyBroadwayAustralia
  3. 3.Division of Zoology, School of Environmental and Rural SciencesUniversity of New EnglandArmidaleAustralia

Personalised recommendations