Abstract
Under 502 nm turquoise light combined with 590 nm yellow light and in total darkness, European robins, Erithacus rubecula, no longer prefer their migratory direction, but exhibit so-called fixed direction responses that do not show the seasonal change between spring and autumn. We tested robins under these light conditions in the local geomagnetic field of 46 μT, a field of twice this intensity, 92 μT, and a field of three times this intensity, 138 μT. Under all three magnetic conditions, the birds preferred the same easterly direction under turquoise-and-yellow light and the same northwesterly direction under dark, while they were oriented in their seasonally appropriate direction under control conditions. “Fixed direction” responses are thus not limited to a narrow intensity window as has been found for normal compass orientation. This can be attributed to their origin in the magnetite-based receptor in the upper beak, which operates according to fundamentally different principles than the radical pair mechanism in the retina mediating compass orientation. “Fixed direction” responses are possibly a relict of a receptor mechanism that changed its function, now mainly providing information on magnetic intensity.
Similar content being viewed by others
References
Batschelet E (1981) Circular statistics in biology. Academic, London
Beason RC, Semm P (1996) Does the avian ophthalmic nerve carry magnetic navigational information? J Exp Biol 199:1241–1244
Davila AF, Fleissner G, Winklhofer M, Petersen N (2003) A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite. Phys Chem Earth 28:647–652
Davila AF, Winklhofer M, Shcherbakov VP, Petersen N (2005) Magnetic pulse affects a putative magnetoreceptor mechanism. Biophys J 89:56–63
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
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 in homing pigeons. Naturwissenschaften 94:631–642
Hanzlik M, Heunemann C, Holzkamp-Rötzler E, Winklhofer M, Petersen N, Fleissner G (2000) Superparamagnetic magnetite in the upper beak tissue of homing pigeons. BioMetals 13:325–331
Holland RA, Kirschvink JL, Doal TG, Wikelski M (2008) Bats use magnetite to detect the earth's magnetic field. PLoS One 3:e1676
Kirschvink JL, Gould JL (1981) Biogenic magnetite as a basis for magnetic field detection in animals. BioSystems 13:181–201
Kirschvink JL, Jones DS, MacFadden BJ (eds) (1985) Magnetite biomineralization and magnetoreception in organisms. Plenum, New York
Marhold S, Wiltschko W, Burda H (1997) A magnetic polarity compass for direction finding in a subterranean mammal. Naturwissenschaften 84:421–423
Muheim R, Bäckman J, Åkesson S (2002) Magnetic compass orientation in European Robins is dependent on both wavelength and intensity of light. J Exp Biol 205:3845–3856
Munro U, Munro JA, Phillips JB, Wiltschko R, Wiltschko W (1997) Evidence for a magnetite-based navigational ‘map’ in birds. Naturwissenschaften 84:26–28
Quinn TP, Brannon EL (1982) The use of celestial and magnetic cues by orienting sockeye salmon smolts. J Comp Physiol 147:547–552
Ritz T, Adem S, Schulten K (2000) A model for photoreceptor-based magnetoreception in birds. Biophys J 78:707–718
Ritz T, Thalau P, Phillips JB, Wiltschko R, Wiltschko W (2004) Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429:177–180
Ritz T, Wiltschko R, Hore PJ, Rodgers CT, Stapput K, Timmel CR, Wiltschko W (2009) Magnetic compass of birds is based on a molecule with optimal directional sensitivity. Biophys J 96:3451–3457
Rogers LJ, Munro U, Freire R, Wiltschko R, Wiltschko W (2008) Lateralized response of chicks to magnetic cues. Behav Brain Res 186:66–71
Shcherbakov VP, Winklhofer M (1999) The osmotic magnetometer: a new model for magnetite-based magnetoreceptors in animals. Eur Biophys J 28:380–392
Solov'yov IA, Greiner W (2007) Theoretical analysis of an iron mineral-based magnetoreceptor model in birds. Biophys J 93:1493–1509
Stapput K, Thalau P, Wiltschko R, Wiltschko W (2008) Orientation of birds in total darkness. Curr Biol 18:602–606
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 92:86–90
Walker MM, Diebel CE, Haugh CV, Pankhurst PM, Montgomery JC, Green CR (1997) Structure and function of the vertebrate magnetic sense. Nature 390:371–376
Wang Y, Pan Y, Parsons S, Walker M, Zhang S (2007) Bats respond to polarity of a magnetic field. Proc R Soc B 274:2901–2905
Wegner RE, Begall S, Burda H (2006) Magnetic compass in the cornea: local anaesthesia impairs orientation in a mammal. J Exp Biol 209:4747–4750
Wiltschko R, Wiltschko W (2009a) ‘Fixed direction’—responses of birds in the geomagnetic field. Commun Integr Biol 2:100–103
Wiltschko R, Wiltschko W (2009b) Directional orientation of birds with the help of the magnetic field under different light conditions. J R Soc Interface (in press)
Wiltschko R, Ritz T, Stapput K, Thalau P, Wiltschko W (2005) Two different types of light-dependent responses to magnetic fields in birds. Curr Biol 15:1518–1523
Wiltschko R, Stapput K, Bischof HJ, Wiltschko W (2007a) Light-dependent magnetoreception in birds: increasing intensity of monochromatic light changes the nature of the response. Front Zool 4:5
Wiltschko R, Stapput K, Ritz T, Thalau P, Wiltschko W (2007b) Magnetoreception in birds: different physical processes for two types of directional responses. HFSP Journal 1:41–47
Wiltschko W (1968) Über den Einfluß statischer Magnetfelder auf die Zugorientierung der Rotkehlchen (Erithacus rubecula). Z Tierpsychol 25:537–558
Wiltschko W (1978) Further analysis of the magnetic compass in migratory birds. In: Schmidt-Koenig K, Keeton WT (eds) Animal migration, navigation and homing. Springer, Berlin, pp 302–310
Wiltschko W, Wiltschko R (1972) Magnetic compass of European robins. Science 176:62–64
Wiltschko W, Wiltschko R (2001) Light-dependent magnetoreception in birds: the behavior of European Robins, Erithacus rubecula, under monochromatic light of various wavelengths. J Exp Biol 204:3295–3302
Wiltschko W, Wiltschko R, Munro U (2000) Light-dependent magnetoreception in birds: the effect of intensity of 565-nm green light. Naturwissenschaften 87:366–369
Wiltschko W, Traudt J, Güntürkün O, Prior H, Wiltschko R (2002) Lateralisation of magnetic compass orientation in a migratory bird. Nature 419:467–470
Wiltschko W, Gesson M, Stapput K, Wiltschko R (2004) Light-dependent magnetoreception in birds: interaction of at least two different receptors. Naturwissenschaften 91:130–134
Wiltschko W, Stapput K, Thalau P, Wiltschko R (2006a) Avian magnetic compass: fast adjustment to intensities outside the normal functional window. Naturwissenschaften 93:300–304
Wiltschko W, Munro U, Ford H, Wiltschko R (2006b) Bird navigation: what type of information does the magnetite-based receptor provide? Proc R Soc B 273:2815–2850
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 210:2300–2310
Wiltschko W, Munro U, Ford H, Wiltschko R (2009) Avian orientation: the pulse effect is mediated by the magnetite receptor in the upper beak. Proc R Soc B 276:2227–2232
Winklhofer M, Holtkamp-Rötzler E, Hanzlik M, Fleissner G, Petersen N (2001) Clusters of superparamagnetic magnetite particles in the upper-beak skin of homing pigeons: evidence of a magnetoreceptor? Eur J Mineral 13:659–669
Acknowledgments
Our work was supported by the Human Frontier Science Program (grant to R.W.) and the Deutsche Forschungsgemeinschaft (grants to R.W. and W.W.). We sincerely thank D. Gehring, J. Klos, Ö. Koc, D. Kringel, J. Raschert, I. Szelecz, and P. Slattery for their valuable help with conducting the experiments. The experiments were performed in accordance with the rules and regulations of animal welfare in Germany.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Tables
(PDF 134 kb)
Rights and permissions
About this article
Cite this article
Wiltschko, W., Dehe, L., Stapput, K. et al. Magnetoreception in birds: no intensity window in “fixed direction” responses. Naturwissenschaften 97, 37–42 (2010). https://doi.org/10.1007/s00114-009-0608-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-009-0608-8