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Magnetic and other non-visual orientation mechanisms in some cave and surface urodeles

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Abstract

Animals adapted to light-deprived habitats might have improved non-visual sensory systems. Specimens of several cave-dwelling species of urodeles spontaneously and persistently align to natural or artificially-modified permanent magnetic fields. Video observations under dim infrared illumination revealed an obvious individual preference for one particular magnetic direction in every animal tested. Therefore, animals changed alignments predictably when the horizontal magnetic field vector (compass direction) was artificially reversed or deviated. When the vertical vector was compensated, individuals aligned axially. With the vertical vector reversed (inclination upward), either axial alignment was still typical, or the individuals behaved as with the horizontal vector reversed. However, reactions as to the natural field occurred as well. The findings suggest a receptor mechanism that needs both horizontal and vertical magnetic cues, but it is still an open question how and where the physical and physiological mechanisms of magnetic transduction and reception are realized. The visual system is likely not necessary because Proteus is ontogenetically deprived of eyesight, and the other species were blindfolded due to the faint infrared illumination. The results therefore tend to favor those putative receptor mechanisms, assumed to work by means of magnetite nano-elements. In sum, the ability to align within the geomagnetic field may be considered a prerequisite for magnetic orientation and is, among other sensory improvements, judged to be highly relevant as an important sensorial and ecological adaptation to light-deprived habitats.

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References

  • Batschelet E (1981) Circular statistics in biology. Academic, London

    Google Scholar 

  • Bulog B, Schlegel P (2000) Functional morphology of the inner ear and underwater audiograms of Proteus anguinus (Amphibia, Urodela). Eur J Physiol 439(Suppl 3):R165–R167

    CAS  Google Scholar 

  • Diego-Rasilla FJ, Lungo RM (2005) Magnetic compass mediates nocturnal homing by the alpine newt, Triturus alpestris. Behav Ecol Sociobiol 58:361–365

    Article  Google Scholar 

  • Fisher JH, Freake MJ, Borland SC, Phillips JB (2001) Evidence for the use of magnetic map information by an amphibian. Anim Behav 62:1–10

    Article  Google Scholar 

  • 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 pigeon. J Comp Neurol 258:350–360

    Article  CAS  Google Scholar 

  • Hanzlik N, Heunemann C, Holztkamp-Rötzler E, Winklhofer M, Fleissner G (2000) Super paramagnetic magnetite in the upper beak tissue of homing pigeons. Biometals 13:325–331

    Article  PubMed  CAS  Google Scholar 

  • Juberthie-Jupeau L (1983) Etude expérimentale de la présence de Coléoptères Bathysciinae souterrains autour de substances alimentaires. Mém Biospéol 10:369–376

    Google Scholar 

  • Lohmann KJ, Lohmann CMF (1994) Acquisition of magnetic directional preference in hatchling loggerhead sea turtles. J Exp Biol 190:1–8

    PubMed  Google Scholar 

  • Lohmann KJ, Johnson S (2000) The neurobiology of magneto reception in vertebrate animals. TINS 23(4):153–159

    PubMed  CAS  Google Scholar 

  • Merkel FW (1980) Orientierung im Tierreich. Fischer, Stuttgart

    Google Scholar 

  • Mittelstaedt H (1982) Einführung in die Kybernetik des Verhaltens am Beispiel der Orientierung im Raum. In: Hoppe W, Lohmann W, Markl H, Ziegler H (eds) Biophysik. Springer, Berlin Heidelberg New York, pp 822–830

    Google Scholar 

  • Papi F, Ioalè P (1988) Pigeon navigation: new experiments on interaction between olfactory and magnetic cues. Comp Biochem Physiol 91A:87–89

    Article  Google Scholar 

  • Phillips JB (1977) Use of the Earth’s magnetic field by orienting cave salamanders (Eurycea lucifuga). J Comp Physiol 121:273–288

    Article  Google Scholar 

  • Phillips JB (1986a) Magnetic compass orientation in the eastern red-spotted newt (Notophthalmus viridescens). J Comp Physiol 158:103–109

    Article  CAS  Google Scholar 

  • Phillips JB (1986b) Two magnetoreception pathways in a migratory salamander. Science 233:765–767

    Article  PubMed  CAS  Google Scholar 

  • Phillips JB (1987) Laboratory studies of homing orientation in the eastern red-spotted newt, Notophthalmus viridescens. J Exp Biol 131:215–229

    PubMed  CAS  Google Scholar 

  • Phillips JB, Borland SC (1992) Magnetic compass orientation is eliminated under near-infrared light in the eastern red-spotted newt Nothophthalmus viridescens. Anim Behav 44:796–797

    Article  Google Scholar 

  • Phillips JB, Adler K, Borland SC (1995) True navigation by an amphibian. Anim Behav 50:855–858

    Article  Google Scholar 

  • Ritz T, Adem S, Schulten K (2000) A model for vision-based magneto reception in birds. Biophys J 78:707–718

    Article  PubMed  CAS  Google Scholar 

  • Roth A, Schlegel P (1988) Behavioral evidence and supporting electrophysiological observations for electro perception in the blind cave Salamander, Proteus anguinus (Urodela). Brain Behav Evol 32:277–280

    Article  PubMed  CAS  Google Scholar 

  • Schlegel P (1996) Behavioral evidence and possible physical and physiological mechanisms for earthmagnetic orientation in the European blind cave Salamander, Proteus anguinus. Mém Biospéol 23:5–16

    Google Scholar 

  • Schlegel PA (1997) Behavioral sensitivity of the European blind cave Salamander, Proteus anguinus, and a Pyrenean Newt, Euproctus asper, to electrical fields in water. Brain Behav Evol 49:121–131

    Article  PubMed  CAS  Google Scholar 

  • Schlegel PA (2006) Spontaneous preferences for magnetic compass direction in the American red spotted newt, Notophthalmus viridescens (Salamandridae, Urodela). J Ethol 25:177–183

    Article  Google Scholar 

  • Schlegel P, Bulog B (1997) Population-specific electro sensitivity of the European blind cave salamander, Proteus anguinus. J Physiol (Paris) 91:275–279

    Google Scholar 

  • Schlegel PA, Roth A (1997) Tuning of electroreceptors in the Blind Cave Salamander, Proteus anguinus L. Brain Behav Evol 49:132–136

    Article  PubMed  CAS  Google Scholar 

  • Schlegel PA, Renner H (2006) Innate preference for magnetic compass direction in the alpine newt, Triturus alpestris (Salamandridae, Urodela)? J Ethol 25:185–193

    Article  Google Scholar 

  • Schlegel PA, Briegleb W, Bulog B, Steinfartz S (2006) Light-sensitivity and non-visual orientation in the blind cave Salamander, Proteus anguinus, and other cave urodele species (in French). Bull Soc Herp Fr 118:1–31

    Google Scholar 

  • Steinfartz S, Veith M, Tautz D (2000) Mitochondrial sequence analysis of Salamandra taxa suggests old splits of major lineages and postglacial recolonizations of central Europe from distinct source populations of Salamandra salamandra. Mol Ecol 9:397–410

    Article  PubMed  CAS  Google Scholar 

  • Steinfartz S, Hwang UW, Tautz D, Öz M, Veith M (2002) Molecular phylogeny of the salamandrid genus Neurergus: evidence for an intrageneric switch of reproductive biology. Amphib-reptil 23:419–431

    Article  Google Scholar 

  • Winklhofer M, Holtkamp-Roetzler E, Hanzlik M, Fleissner G, Petersen N (2001) Clusters of super paramagnetic particles in the upper-beak skin of homing pigeons: evidence of a magneto receptor? Eur J Mineral 13:659–669

    Article  CAS  Google Scholar 

  • Wiltschko W, Merkel FW (1966) Orientierung zugunruhiger Rotkehlchen im statischen Magnetfeld. Verh Dtsch Zool Ges 59:362–367

    Google Scholar 

  • Wiltschko W (1968) Über den Einfluß statischer Magnetfelder auf die Zugorientierung der Rotkehlchen (Erithacus rubecula). Z Tierpsychol 25:537–558

    PubMed  CAS  Google Scholar 

  • Wiltschko R, Wiltschko W (1995) Magnetic orientation in animals. Zoophysiology, vol. 33. Springer, Berlin

    Google Scholar 

  • Wiltschko R, Wiltschko W (2003) Avian navigation: from historical to modern concepts. Anim Behav 65:257–272

    Article  Google Scholar 

  • Wiltschko W, Wiltschko R (2005) Magnetic orientation and magneto reception in birds and other animals. J Comp Physiol A 191:675–693

    Article  Google Scholar 

Download references

Acknowledgments

The stay of the author in Moulis was partly sponsored by the program PROCOPE (German federal government for foreign affairs) and grants of the „Bayrisch-Französisches Hochschulzentrum”. I am very much indebted to the French counterpart of this exchange program, the directors of the “Laboratoire Souterrain”, Drs Ch. Juberthie, J. Durand, and A. Mangin (CNRS-Moulis), who originally invited me for these stays and helped me essentially with their background knowledge and the facilities offered of the laboratory and by its staff. For discussions and valuable suggestions, I thank Drs P.B. Richard, C. Juberthie, J. Durand, M. Beblo (who also provided two Helmholtz-coils for the laboratory cave and valuable Earth’s magnetic and geophysical knowledge), W. Briegleb, G. and G. Fleissner, and R. and W. Wiltschko. Comments on earlier versions of the manuscript by B. Beason, M. Winklhofer, E. Holtzkamp-Rötzler, and R. Thomsen were especially helpful and appreciated. I particularly thank Dr. Ch. Pavey for suggestions to the manuscript and for correcting the English of an earlier version of this manuscript and Dr. Les Williams for polishing the English in the last version. The specimens of Desmognathus were obtained by courtesy from Prof. Dr. G. Roth, Dr. U. Diecke, and Dr. W. Grunwald, Univ. of Bremen. A statistical “adopted homogeneity test” was designed and done by A. von Haeseler and is very much appreciated.

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  1. Peter A. Schlegel

    Present address: Dept. Biologie II, Biozentrum, Ludwig-Maximilians-Universität, Grosshadenerstr. 2, 82152, Planegg–Martinsried, Germany

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  1. Laboratoire Souterrain, CNRS, 09200, Moulis–St Girons, France

    Peter A. Schlegel

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Correspondence to Peter A. Schlegel.

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Schlegel, P.A. Magnetic and other non-visual orientation mechanisms in some cave and surface urodeles. J Ethol 26, 347–359 (2008). https://doi.org/10.1007/s10164-007-0071-y

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  • DOI: https://doi.org/10.1007/s10164-007-0071-y

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