Magnetoreception in the wood mouse (Apodemus sylvaticus): influence of weak frequency-modulated radio frequency fields
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.
PubMed
25923312
PubMed Central
PMC4413948
DOI
10.1038/srep09917
PII: srep09917
Knihovny.cz E-zdroje
- MeSH
- čití, cítění fyziologie MeSH
- elektromagnetické záření MeSH
- hnízdění fyziologie MeSH
- magnetické pole * MeSH
- Murinae fyziologie MeSH
- orientace fyziologie MeSH
- rádiové vlny MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
The mammalian magnetic sense is predominantly studied in species with reduced vision such as mole-rats and bats. Far less is known about surface-dwelling (epigeic) rodents with well-developed eyes. Here, we tested the wood mouse Apodemus sylvaticus for magnetoreception using a simple behavioural assay in which mice are allowed to build nests overnight in a visually symmetrical, circular arena. The tests were performed in the ambient magnetic field or in a field rotated by 90°. When plotted with respect to magnetic north, the nests were bimodally clustered in the northern and southern sectors, clearly indicating that the animals used magnetic cues. Additionally, mice were tested in the ambient magnetic field with a superimposed radio frequency magnetic field of the order of 100 nT. Wood mice exposed to a 0.9 to 5 MHz frequency sweep changed their preference from north-south to east-west. In contrast to birds, however, a constant frequency field tuned to the Larmor frequency (1.33 MHz) had no effect on mouse orientation. In sum, we demonstrated magnetoreception in wood mice and provide first evidence for a radical-pair mechanism in a mammal.
Department of Biological Sciences Virginia Tech Blacksburg Virginia United States of America
Department of Earth and Environmental Sciences Geophysics Munich University 80333 Munich Germany
Department of General Zoology Faculty of Biology University of Duisburg Essen 45117 Essen Germany
Zobrazit více v PubMed
Wiltschko R. & Wiltschko W. in Sensing in Nature. (ed López-Larrea C., ed. ) 126–141 (Springer, 2012).
Wiltschko R. & Wiltschko W. Avian magnetic compass: Its functional properties and physical basis. Current Zoology 56, 265–276 (2010).
Phillips J. B. Magnetic compass orientation in the eastern red-spotted newt (Notophthalmus viridescens). J. Comp. Physiol. A. 158, 103–109 (1986). PubMed
Phillips J. B. Two magnetoreception pathways in a migratory salamander. Science 233, 765–767 (1986). PubMed
Lohmann K. J., Lohman C. M. F., Ehrhart L. M., Bagley D. A. & Swing T. Geomagnetic map used in sea–turtle navigation. Nature 428, 909–910 (2004). PubMed
Kirschvink J. L., Walker M. M. & Diebel C. E. Magnetite-based magnetoreception. Curr. Opin. Neurobiol. 11, 462–467 (2001). PubMed
Kobayashi A. & Kirschvink J. L. in Electromagnetic Fields: Biological Interactions and Mechanisms. (ed Blank M., ed. ) 367–394 (American Chemical Society Books, 1995).
Begall S., Burda H. & Malkemper E. P. in Adv. Study Behav. Vol. 46 (ed Naguib M., ed. ) 45–88 (Elsevier, 2014).
August P. V., Ayvazian S. G. & Anderson J. G. T. Magnetic orientation in a small mammal, Peromyscus leucopus. J. Mammal. 70, 1–9 (1989).
Mather J. G. & Baker R. R. Magnetic sense of direction in woodmice for route-based navigation. Nature 291, 152–155 (1981).
Madden R. C. & Phillips J. B. An attempt to demonstrate magnetic compass orientation in two species of mammals. Learn. Behav. 15, 130–134 (1987).
Sauvé J. P. Analyse de l’orientation initiale dans une expérience de retour au gîte chez le mulot, Apodemus sylvaticus. Sciences et Techniques de l’Animal de Laboratoire 13, 89–91 (1988).
Burda H., Marhold S., Westenberger T., Wiltschko R. & Wiltschko W. Evidence for magnetic compass orientation in the subterranean rodent Cryptomys hottentotus (Bathyergidae). Experientia 46, 528–530 (1990). PubMed
Oliveriusová L., Němec P., Králová Z. & Sedláček F. Magnetic compass orientation in two strictly subterranean rodents: learned or species-specific innate directional preference? J. Exp. Biol. 215, 3649–3654 (2012). PubMed
Oliveriusová L., Němec P., Pavelková Z. & Sedláček F. Spontaneous expression of magnetic compass orientation in an epigeic rodent: the bank vole, Clethrionomys glareolus. Naturwissenschaften 101, 557–563 (2014). PubMed
Thalau P., Ritz T., Burda H., Wegner R. E. & Wiltschko R. The magnetic compass mechanisms of birds and rodents are based on different physical principles. J. R. Soc. Interface 3, 583–587 (2006). PubMed PMC
Wegner R. E., Begall S. & Burda H. Magnetic compass in the cornea: local anaesthesia impairs orientation in a mammal. J. Exp. Biol. 209, 4747–4750 (2006). PubMed
Muheim R., Edgar N. M., Sloan K. A. & Phillips J. B. Magnetic compass orientation in C57BL/6J mice. Learn. Behav. 34, 366–373 (2006). PubMed
Marhold S., Beiles A., Burda H. & Nevo E. Spontaneous directional preference in a subterranean rodent, the blind mole-rat, Spalax ehrenbergi. Folia Zool. 49, 7–18 (2000).
Burda H. et al. Magnetic orientation in subterranean mole rats of the superspecies Spalax ehrenbergi: Experiments, patterns, and memory. Isr. J. Zool. 37, 182–183 (1991).
Marhold S., Wiltschko W. & Burda H. A magnetic polarity compass for direction finding in a subterranean mammal. Naturwissenschaften 84, 421–423 (1997).
Deutschlander M. E. et al. Learned magnetic compass orientation by the Siberian hamster, Phodopus sungorus. Anim. Behav. 65, 779–786 (2003).
Kirschvink J. L. & Gould J. L. Biogenic magnetite as a basis for magnetic field detection in animals. Biosystems 13, 181–201 (1981). PubMed
Davila A. F., Fleissner G., Winklhofer M. & Petersen N. A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite. Phys. Chem. Earth 28, 647–652 (2003).
Shcherbakov V. P. & Winklhofer M. Theoretical analysis of flux amplification by soft magnetic material in a putative biological magnetic-field receptor. Phys. Rev. E. 81, 031921 (2010). PubMed
Winklhofer M. & Kirschvink J. L. A quantitative assessment of torque-transducer models for magnetoreception. J. R. Soc. Interface 7, 273–289, 10.1098/rsif.2009.0435.focus (2010). PubMed DOI PMC
Dodson C. A., Hore P. & Wallace M. I. A radical sense of direction: signalling and mechanism in cryptochrome magnetoreception. Trends Biochem. Sci. 38, 435–446, http://dx.doi.org/10.1016/j.tibs.2013.07.002 (2013). PubMed DOI
Ritz T., Ahmad M., Mouritsen H., Wiltschko R. & Wiltschko W. Photoreceptor-based magnetoreception: optimal design of receptor molecules, cells, and neuronal processing. J. R. Soc. Interface 7, 135–146 (2010). PubMed PMC
Ritz T., Adem S. & Schulten K. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707–718 (2000). PubMed PMC
Wiltschko W. & Wiltschko R. The magnetic compass of European robins. Science 176, 62–64 (1972). PubMed
Wiltschko R. & Wiltschko W. The magnetite-based receptors in the beak of birds and their role in avian navigation. J. Comp. Physiol. A 199, 89–98 (2012). PubMed PMC
Marhold S., Burda H., Kreilos I. & Wiltschko W. in RIN 97 Orientation & Navigation - Birds, Humans and Other Animals. 1–9 (Royal Institute of Navigation London).
Holland R. A., Kirschvink J. L., Doak T. G. & Wikelski M. Bats use magnetite to detect the Earth's magnetic field. PLoS. ONE 3, e1676 (2008). PubMed PMC
Keary N. et al. Oscillating magnetic field disrupts magnetic orientation in Zebra finches, Taeniopygia guttata. Front. Zool. 6, 25 (2009). PubMed PMC
Ritz T., Thalau P., Phillips J. B., Wiltschko R. & Wiltschko W. Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429, 177–180 (2004). PubMed
Rodgers C. T. & Hore P. J. Chemical magnetoreception in birds: the radical pair mechanism. Proc. Natl. Acad. Sci. U.S.A. 106, 353–360 (2009). PubMed PMC
Stapput K., Thalau P., Wiltschko R. & Wiltschko W. Orientation of birds in total darkness. Curr. Biol. 18, 602–606 (2008). PubMed
Thalau P., Ritz T., Stapput K., Wiltschko R. & Wiltschko W. Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften 92, 86–90 (2005). PubMed
Engels S. et al. Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird. Nature 509, 353–356, 10.1038/nature13290 (2014). PubMed DOI
Phillips J. B. et al. Rapid learning of magnetic compass direction by C57BL/6 mice in a 4-armed ‘plus’ water maze. PLoS. ONE 8, e73112, 10.1371/journal.pone.0073112 (2013). PubMed DOI PMC
Tew T. E. & MacDonald D. W. Dynamics of space use and male vigour amongst wood mice, Apodemus sylvaticus, in the cereal ecosystem. Behav. Ecol. Sociobiol. 34, 337–345 (1994).
Hacker H. P. & Pearson H. S. Distribution of the long-tailed field mouse, Apodemus sylvaticus, on South Haven Peninsula, Dorset, in 1937, with some observations on its wandering and homing powers. J. Proc. Linn. Soc., Zool. 42, 1–17, 10.1111/j.1096-3642.1951.tb01850.x (1951). DOI
Jamon M. & Bovet P. Possible use of environmental gradients in orientation by homing wood mice, Apodemus sylvaticus. Behav. Process. 15, 93–107, http://dx.doi.org/10.1016/0376-6357(87)90035-0 (1987). PubMed DOI
Begall S., Malkemper E. P., Červený J., Němec P. & Burda H. Magnetic alignment in mammals and other animals. Mamm. Biol. 78, 10–20, http://dx.doi.org/10.1016/j.mambio.2012.05.005 (2013). DOI
Begall S., Červený J., Neef J., Vojtěch O. & Burda H. Magnetic alignment in grazing and resting cattle and deer. Proceedings of the National Academy of Sciences 105, 13451–13455 (2008). PubMed PMC
Hart V. et al. Dogs are sensitive to small variations of the Earth's magnetic field. Front. Zool. 10, 80 (2013). PubMed PMC
Ritz T. et al. Magnetic compass of birds is based on a molecule with optimal directional sensitivity. Biophys. J. 96, 3451–3457 (2009). PubMed PMC
Schulten K., Swenberg C. & Weller A. A biomagnetic sensory mechanism based on the geminate recombination of radical ion pairs in solvents. J. Phys. Chem. NF101, 371–390 (1978).
Xu B.-M., Zou J., Li H., Li J.-G. & Shao B. Effect of radio frequency fields on the radical pair magnetoreception model. Phys. Rev. E. 90, 042711 (2014). PubMed
Lambert N., De Liberato S., Emary C. & Nori F. Radical-pair model of magnetoreception with spin-orbit coupling. New J. Phys. 15, 083024 (2013).
Nießner C. et al. Avian ultraviolet/violet cones identified as probable magnetoreceptors. PLoS. ONE 6, e20091 (2011). PubMed PMC
Nießner C. et al. Magnetoreception: activated cryptochrome 1a concurs with magnetic orientation in birds. J. R. Soc. Interface 10, 20130638, 10.1098/rsif.2013.0638 (2013). PubMed DOI PMC
Solov'yov I. A. & Schulten K. Magnetoreception through cryptochrome may involve superoxide. Biophys. J. 96, 4804–4813 (2009). PubMed PMC
Lee A. A. et al. Alternative radical pairs for cryptochrome-based magnetoreception. J. R. Soc. Interface 11, 10.1098/rsif.2013.1063 (2014). PubMed DOI PMC
Wiltschko R., Stapput K., Thalau P. & Wiltschko W. Directional orientation of birds by the magnetic field under different light conditions. J. R. Soc. Interface 7, S163–S177 (2010). PubMed PMC
Landler L., Painter M. S., Youmans P. W., Hopkins W. A. & Phillips J. B. Spontaneous magnetic alignment by yearling snapping turtles: rapid association of radio frequency dependent pattern of magnetic input with novel surroundings. PLoS. ONE. in press (2015). PubMed PMC
Gauger E. M., Rieper E., Morton J. J. L., Benjamin S. C. & Vedral V. Sustained quantum coherence and entanglement in the avian compass. Phys. Rev. Lett. 106, 040503 (2011). PubMed
Phillips J. B., Muheim R. & Jorge P. E. A behavioral perspective on the biophysics of the light-dependent magnetic compass: a link between directional and spatial perception? J. Exp. Biol. 213, 3247–3255 (2010). PubMed
Červený J., Begall S., Koubek P., Nováková P. & Burda H. Directional preference may enhance hunting accuracy in foraging foxes. Biol. Lett. 7, 355–357, 10.1098/rsbl.2010.1145 (2011). PubMed DOI PMC
Hart V. et al. Directional compass preference for landing in water birds. Front. Zool. 10, 38 (2013). PubMed PMC
Kirschvink J. L. et al. in Sensory Transduction. (eds Corey D. P., & Roper S. D., eds. ) 225–240. (Society of General Physiologists, 45th Annual Symposium, Rockefeller University Press, 1992).
Fleissner G., Stahl B., Thalau P. & Falkenberg G. A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons. Naturwissenschaften 94, 631–642 (2007). PubMed
ICNIRP. . in Health Phys Vol. 74 (ed International Commission for Non-Ionizing Radiation Protection.) 494–522 (1998). PubMed
Kirschvink J. L. Uniform magnetic fields and double wrapped coil systems: Improved techniques for the design of bioelectromagnetic experiments. Bioelectromagnetics 13, 401–411 (1992). PubMed
Batschelet E. Circular Statistics in Biology. (Academic Press., 1981).
Eyes are essential for magnetoreception in a mammal
Magnetic alignment enhances homing efficiency of hunting dogs
Weak radiofrequency fields affect the insect circadian clock
Dogs can be trained to find a bar magnet
Cryptochrome 1 in Retinal Cone Photoreceptors Suggests a Novel Functional Role in Mammals