The magnetic sense and its use in long-distance navigation by animals

Current Opinion in Neurobiology

Volumn 12, Issue 6, 2002, Pages 735-744

  Walker, Michael M ^a   Dennis, Todd E ^a   Kirschvink, Joseph L ^b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; BIRD; FLYING; MAGNETIC FIELD; MAGNETORECEPTOR; MODEL; NONHUMAN; PERCEPTION; PREDICTION; PRIORITY JOURNAL; PROPRIOCEPTION; REVIEW; SENSORY RECEPTOR; SIGNAL PROCESSING; SPATIAL ORIENTATION;

EID: 0036904716     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(02)00389-6     Document Type: Review

References (51)

1. Griffin D.R. Ecology of migration; is magnetic orientation a reality? Quart Rev Biol. 57:1982;293-295.
2. Viguier C. Le sense d'orientation et ses organes chez les animaux et chez l'homme. Rev Phil France Étranger. 14:1882;1-36. [Title translation: The senses of orientation and their organs in animals and men.].
3. Kramer G. Wird die Sonnenhöhe bei der Heimfindeorientierung verwertet? J Ornithol. 94:1953;201-219. [Title translation: Does information about the height of the sun play a role in navigation/homing behaviour?].
4. Wiltschko R., Wiltschko W. Magnetic orientation in animals. Zoophysiology. 33:1995;Springer, Berlin.
5. Gould J.L. The map sense of pigeons. Nature. 296:1982;205-211. The author reviews the competing hypotheses of position determination by homing pigeons using either wind-borne odours or the Earth's magnetic field. He concludes that both hypotheses suffer from failure to identify a second independent coordinate for use in position determination. (See also the ensuing discussion of this paper in Nature 1982, 300:293-294.).
6. Schmidt-Koenig K., Walcott C. Tracks of pigeons homing with frosted lenses. Anim Behav. 26:1978;480-486.
7. Walcott C., Schmidt-Koenig K. The effect on pigeon homing of anesthesia during displacement. The Auk. 90:1973;281-286.
8. Skiles D.D. The geomagnetic field: its nature, history and biological relevance. Kirschvink J.L., Jones D.S., MacFadden B.J. Magnetite Biomineralization and Magnetoreception by Living Organisms: A New Biomagnetism. 1985;43-102 Plenum Publishing Corporation, New York. The author provides a comprehensive review of the properties of the Earth's magnetic field that is easily accessible for biologists. Properties of the Earth's field constrain uses of the magnetic field for orientation in both space and time. These constraints must be understood when considering models of position determination during navigation by animals travelling over long distances.
9. Kirschvink J.L., Walker M.M., Diebel C.E. Magnetite-based magnetoreception. Curr Opin Neurobiol. 11:2001;462-467.
10. Kirschvink J.L., Gould J.L. Biogenic magnetite as a basis for magnetic field detection in animals. Biosystems. 13:1981;181-201.
11. Kirschvink J.L., Walker M.M. Particle-size considerations for magnetite-based magnetoreceptors. Kirschvink J.L., Jones D.S., MacFadden B.J. Magnetite Biomineralization and Magnetoreception by Living Organisms: A New Biomagnetism. 1985;243-254 Plenum Publishing Corporation, New York. The authors show how magnetite can be used to measure the magnetic field vector and can provide the basis for understanding long-distance navigation in terms of the events occurring in single receptor cells. The authors also predict the likely magnetic-to-thermal energy ratios of magnetite chains used to detect magnetic field direction and intensity.
12. Walker M.M., Diebel C.E., Haugh C.V., Pankhurst P.M., Montgomery J.C., Green C.R. Structure and function of the vertebrate magnetic sense. Nature. 390:1997;371-376. This paper provides the first demonstration of the key elements of the magnetic sense - candidate magnetite-based magnetoreceptor cells [13], coupled with neural and behavioural responses to magnetic field stimuli - in a single species, the rainbow trout. The candidate magnetoreceptor cells are located in the olfactory lamellae in the nose and are closely associated with fine branches of the superficial ophthalmic branch of the trigeminal nerve. A clear implication of the results presented in the paper is that pigeon homing experiments in which pigeons are made anosmic [5••] are very likely to be confounded by simultaneous impairment of the magnetic sense.
13. Diebel C.E., Proksch R., Green C.R., Neilson P., Walker M.M. Magnetite defines a magnetoreceptor. Nature. 406:2000;299-302.
14. Kirschvink J.L. Comment on 'Constraints on biological effects of weak extemely-low-frequency electromagnetic fields'. Phys Rev A. 46:1992;2178-2184.
15. Kirschvink J.L., Padmanabha S., Boyce C.K., Oglesby J. Measurement of the threshold sensitivity of honeybees to weak, extremely low-frequency magnetic fields. J Exp Biol. 200:1997;1363-1368.
16. Irwin W.P., Lohmann K.J. Orientation behavior of sea turtle hatchlings: disruption by magnets. Am Zool. 39:2000;125A. [Also see online poster at http://www.unc.edu/depts/geomag/ ].
17. Walker M.M., Bitterman M.E. Attached magnets disrupt magnetic field discrimination by honeybees. J Exp Biol. 141:1988;447-451.
18. Keeton W.T. Magnets interfere with pigeon homing. Proc Natl Acad Sci USA. 68:1971;102-106.
19. Visalberghi E., Alleva E. Magnetic influences on pigeon homing. Biol Bull. 156:1979;246-256.
20. Lednor A.J., Walcott C. Homing pigeon navigation: the effects of in-flight exposure to a varying magnetic field. Comp Biochem Physiol A. 76:1983;655-671.
21. Wiltschko W., Nohr D., Füller E., Wiltschko R. Pigeon homing: the use of magnetic information in position finding. Maret G., Boccara N., Kiepenheuer J. Biophysical Effects of Steady Magnetic Fields. 1986;154-162 Springer, Berlin.
22. Becker M., Füller E., Wiltschko R. Pigeon orientation: daily variation between morning and noon occur in some years but not in others. Naturwiss. 78:1991;426-428.
23. Walker M.M., Bitterman M.E. Honeybees can be trained to respond to very small changes in geomagnetic field intensity. J Exp Biol. 145:1989;489-494.
24. Semm P., Beason R.C. Responses to small magnetic field variations by the trigeminal system of the bobolink. Brain Res Bull. 25:1990;735-740.
25. Keeton W.T., Larkin T.S., Walcott C., Windsor D.M. Normal fluctuations in the earth's field influence pigeon orientation. J Comp Physiol. 95:1974;95-103.
26. Walcott C. Anomalies in the Earth's Magnetic Field increase the scatter of pigeons' vanishing bearings. Schmidt-Koenig K., Keeton W.T. Animal Migration, Navigation, and Homing. 1978;143-151 Springer Verlag, Berlin.
27. Klimley A.P. Highly directional swimming by scalloped hammerhead sharks, Sphyrna lewini, and substrate irradiance, temperature, bathymetry and geomagnetic field. Mar Biol. 117:1993;1-22.
28. Kirschvink J.L., Dizon A.E., Westphal J.A. Evidence from strandings for geomagnetic sensitivity in cetaceans. J Exp Biol. 120:1986;1-24. Magnetic anomalies produced by seafloor spreading create a pattern of linear magnetic 'ridges' and 'valleys' trending predominantly north-south in the Atlantic and Pacific Oceans. The authors note that animals might use these patterns to guide movement during migration by following either the ridges or the valleys and show that the locations where whales strand themselves alive are highly correlated with places where magnetic valleys intersect the coastline.
29. Kirschvink J.L. Geomagnetic sensitivity in cetaceans: an update with live stranding records in the United States. Thomas J.A., Kastelein R.A. Sensory Abilities of Cetaceans Laboratory and Field Evidence. 1990;639-649 Plenum Publishing Corporation, New York.
30. Walker M.M., Kirschvink J.L., Ahmed G., Dizon A.E. Fin whales (Balaenoptera physalus) avoid geomagnetic gradients during migration. J Exp Biol. 171:1992;67-78.
31. Quinn T.P. An experimental approach to fish compass and map orientation. Cleave J.D., Arnold G.P., Dodson J.J., Neill W.H. Mechanisms of Migration in Fishes. 1984;113-123 Plenum Publishing Corporation, New York.
32. Lohmann K.J., Lohmann C.M.F. Detection of magnetic field intensity by sea turtles. Nature. 380:1996;59-61. On the basis of laboratory orientation experiments with hatchling sea turtles, the authors propose in this and related papers that sea turtles might either navigate using the inclination and intensity of the Earth's field as a pair of coordinates, or be genetically programmed to recognise key locations in their habitat (see also [33-36]).
33. Lohmann K.J., Lohmann C.M.F. Orientation and open-sea navigation in sea turtles. J Exp Biol. 199:1996;73-81.
34. Lohmann K.J. Magnetic orientation by hatchling loggerhead sea turtles. J Exp Biol. 155:1991;37-49.
35. Lohmann K.J., Lohmann C.M.F. Detection of magnetic inclination by sea turtles: a possible mechanism for determining latitude. J Exp Biol. 194:1994;23-32.
36. Lohmann K.J., Cain S.D., Dodge S.A., Lohmann C.M.F. Regional magnetic fields as navigational markers for sea turtles. Science. 294:2001;364-366.
37. Lohmann K.J., Hester J.T., Lohmann C.M.F. Long-distance navigation in sea turtles. Ethol Ecol Evol. 11:1999;1-23.
38. Akesson S., Alerstam T. Oceanic navigation: are there any feasible geomagnetic bi-coordinate combinations for albatrosses. J Avian Biol. 29:1998;618-625.
39. Courtillot V., Hulot G., Alexandrescu M., le Mouel J.-L., Kirschvink J.L. Sensitivity and evolution of sea-turtle magnetoreception: observations, modelling and constraints from geomagnetic secular variation. Terra Nova. 9:1997;203-207.
40. Walker M.M. On a wing and a vector: a model for magnetic navigation by homing pigeons. J Theor Biol. 192:1998;341-349. The author uses a pattern recognised in previously published pigeon orientation data as the basis for a model for position determination using two coordinates derived from the main magnetic field of the Earth. The model explains a considerable volume of previously published pigeon orientation data (also of interest [39]) and makes testable predictions concerning the behaviour of pigeons at release sites.
41. Walker M.M. Magnetic position determination by homing pigeons. J Theor Biol. 197:1999;271-276.
42. Walker M.M., Kirschvink J.L., Kirschvink A.K. A mathematical model for navigation by animals. Maret G., Boccara N., Kiepenheuer J. Biophysical effects of steady magnetic fields. 1986;207-211 Springer, Berlin.
43. Wallraff H.G. The magnetic map of homing pigeons: an evergreen phantom. J Theor Biol. 197:1999;265-269.
44. Lednor A.J., Walcott C. Orientation of homing pigeons at magnetic anomalies: the effects of experience. Behav Ecol Sociobiol. 22:1988;3-8.
45. Vine F.J., Matthews D.H. Magnetic anomalies over oceanic ridges. Nature. 199:1963;947-949.
46. Vine F.J. Spreading of the ocean floor; new evidence. Science. 154:1966;1405-1415.
47. Vine F.J. Magnetic anomalies associated with mid-ocean ridges. Phinney R.A. The History of the Earth's Crust; a Symposium. 1968;Princeton University Press, Princeton, NJ.
48. Steiner I., Clemens B., Werfelli S., Dell'Omo G., Valenti P., Troester G., Wolfer D.P., Lipp H.-P. A GPS logger and software for analysis of homing in pigeons and small mammals. Physiol Behav. 71:2000;589-596.
49. von Hünerbein K., Hamann H.-J., Rueter E., Wiltschko W. A GPS-based system for recording the flight paths of birds. Naturwiss. 87:2000;278-279.
50. Windsor D.M. Regional expression of directional preferences by experienced homing pigeons. Anim Behav. 23:1975;335-343.
51. Müller R.D., Roest W.R., Royer J.-Y., Gahagan L.M., Sclater J.G. Digital isochrons of the World's ocean floor. J Geophys Res. 102:1997;3211-3214.