For centuries, humans have been fascinated by how migratory animals find their way over thousands of kilometres. Here, I review the mechanisms used in animal orientation and navigation with a particular focus on long-distance migrants and magnetoreception. I contend that any long-distance navigational task consists of three phases and that no single cue or mechanism will enable animals to navigate with pinpoint accuracy over thousands of kilometres. Multiscale and multisensory cue integration in the brain is needed. I conclude by raising twenty important mechanistic questions related to long-distance animal navigation that should be solved over the next twenty years.
This is a preview of subscription content
Subscription info for Chinese customers
We have a dedicated website for our Chinese customers. Please go to naturechina.com to subscribe to this journal.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Wiltschko, R. & Wiltschko, W. Magnetic Orientation in Animals (Springer, Berlin, 1995). This book is an exhaustive account of almost all studies related to magnetoreception in any animal published before 1995, and it is a valuable historical account of the early achievements in the field.
Berthold, P. A comprehensive theory for the evolution, control and adaptability of avian migration. Ostrich 70, 1–11 (1999).
Mouritsen, H. in Avian Migration (eds Berthold, P., Gwinner, E. & Sonnenschein, E.) 493–513 (Springer, Berlin, 2003).
Mouritsen, H. in Sturkie’s Avian Physiology (ed. Scanes, C.) 113–133 (Elsevier, Amsterdam, 2015).
Schmaljohann, H., Fox, J. W. & Bairlein, F. Phenotypic response to environmental cues, orientation and migration costs in songbirds flying halfway around the world. Anim. Behav. 84, 623–640 (2012).
Salewski, V., Bairlein, F. & Leisler, B. Recurrence of some palaearctic migrant passerine species in West Africa. Ring. Migr. 20, 29–30 (2000).
Gill, R. E. Jr et al. Extreme endurance flights by landbirds crossing the Pacific Ocean: ecological corridor rather than barrier? Proc. R. Soc. Lond. B 276, 447–457 (2009).
Egevang, C. et al. Tracking of Arctic terns Sterna paradisaea reveals longest animal migration. Proc. Natl Acad. Sci. USA 107, 2078–2081 (2010).
Jouventin, P. & Weimerskirch, H. Satellite tracking of wandering albatrosses. Nature 343, 746–748 (1990).
Gagliardo, A. et al. Oceanic navigation in Cory’s shearwaters: evidence for a crucial role of olfactory cues for homing after displacement. J. Exp. Biol. 216, 2798–2805 (2013). This paper convincingly showed that olfactory information is essential for long-distance homing in Cory’s shearwaters, because birds fitted with satellite transmitters and released about 800 km from home with their olfactory nerves cut wandered aimlessly around the Atlantic Ocean, whereas shearwaters with intact olfactory nerves but with cut ophthalmic branches of the trigeminal nerves went straight home.
Brower, L. Monarch butterfly orientation: missing pieces of a magnificent puzzle. J. Exp. Biol. 199, 93–103 (1996).
Mouritsen, H. & Frost, B. J. Virtual migration in tethered flying monarch butterflies reveals their orientation mechanisms. Proc. Natl Acad. Sci. USA 99, 10162–10166 (2002).
Zeil, J. Visual homing: an insect perspective. Curr. Opin. Neurobiol. 22, 285–293 (2012).
Wehner, R., Cheng, K. & Cruse, H. in The New Visual Neurosciences 1153–1164 (MIT Press, Cambridge, 2014).
Bech, M., Homberg, U. & Pfeiffer, K. Receptive fields of locust brain neurons are matched to polarization patterns of the sky. Curr. Biol. 24, 2124–2129 (2014). This elegant electrophysiological paper used the scientific advantage of the simplicity of the insect brain to show that some neurons in the central complex of locusts seem to be matched filters to the natural polarization pattern, so that different cells respond to different orientations of the complete celestial polarization pattern across the dome of the sky, and that these neurons can differentiate between solar and antisolar directions based only on the polarization pattern.
Heinze, S. Neuroethology: unweaving the senses of direction. Curr. Biol. 25, R1034–R1037 (2015).
Chapman, J. W., Reynolds, D. R. & Wilson, K. Long-range seasonal migration in insects: mechanisms, evolutionary drivers and ecological consequences. Ecol. Lett. 18, 287–302 (2015).
Warrant, E. et al. The Australian bogong moth Agrotis infusa: a long-distance nocturnal navigator. Front. Behav. Neurosci. 10, 77 (2016).
Chapman, J. W. et al. Wind selection and drift compensation optimize migratory pathways in a high-flying moth. Curr. Biol. 18, 514–518 (2008). This paper was the first to show that high-flying insects are not at the mercy of the wind but that they actively orient themselves in mid-air and that they choose favourable airstreams that enable them to perform directed migration in spring and return migration in autumn; this paper therefore also disproved the ‘pied piper’ hypothesis that high-flying insects were blown in random directions.
Chapman, J. W. et al. Flight orientation behaviors promote optimal migration trajectories in high-flying insects. Science 327, 682–685 (2010).
Hu, G. et al. Mass seasonal bioflows of high-flying insect migrants. Science 354, 1584–1587 (2016).
Lohmann, K. J., Cain, S. D., Dodge, S. A. & Lohmann, C. M. F. Regional magnetic fields as navigational markers for sea turtles. Science 294, 364–366 (2001).
Putman, N. F. et al. Evidence for geomagnetic imprinting as a homing mechanism in Pacific salmon. Curr. Biol. 23, 312–316 (2013). This elegant paper used fisheries data and information on geomagnetic field drift to demonstrate that Pacific salmon returning to spawn had imprinted on the geomagnetic parameters of their natal river mouth before they left the area years earlier.
Brothers, J. R. & Lohmann, K. J. Evidence for geomagnetic imprinting and magnetic navigation in the natal homing of sea turtles. Curr. Biol. 25, 392–396 (2015).
Bett, N. N. & Hinch, S. G. Olfactory navigation during spawning migrations: a review and introduction of the hierarchical navigation hypothesis. Biol. Rev. Camb. Philos. Soc. 91, 728–759 (2016).
Gerlach, G., Atema, J., Kingsford, M. J., Black, K. P. & Miller-Sims, V. Smelling home can prevent dispersal of reef fish larvae. Proc. Natl Acad. Sci. USA 104, 858–863 (2007). This paper used genetic fingerprinting and behavioural tests to elegantly demonstrate that returning reef fish larvae are attracted to the odour of their natal reef, that they can discriminate this odour from the odour of other reefs, and that this olfactory imprinting on their natal reef might help explain the high levels of retention and speciation in coral reefs.
Mouritsen, H., Atema, J., Kingsford, M. J. & Gerlach, G. Sun compass orientation helps coral reef fish larvae return to their natal reef. PLoS One 8, e66039 (2013).
Bottesch, M. et al. A magnetic compass that might help coral reef fish larvae return to their natal reef. Curr. Biol. 26, R1266–R1267 (2016).
Alerstam, T. et al. Convergent patterns of long-distance nocturnal migration in noctuid moths and passerine birds. Proc. R. Soc. Lond. B 278, 3074–3080 (2011).
Lohmann, K. J., Lohmann, C. M. F., Brothers, J. R. & Putman, N. F. in The Biology of Sea Turtles (eds Wyneken, J., Lohmann, K. J. & Musick, J. A.) vol. 3, 59–77 (CRC Press, Boca Raton, 2013).
Holland, R. A. True navigation in birds: from quantum physics to global migration. J. Zool. (Lond.) 293, 1–15 (2014).
Mouritsen, H., Heyers, D. & Güntürkün, O. The neural basis of long-distance navigation in birds. Annu. Rev. Physiol. 78, 133–154 (2016).
Phillips, J. B. Two magnetoreception pathways in a migratory salamander. Science 233, 765–767 (1986).
Guilford, T. & Biro, D. Route following and the pigeon’s familiar area map. J. Exp. Biol. 217, 169–179 (2014).
Griffin, D. R. Bird navigation. Biol. Rev. Camb. Philos. Soc. 27, 359–400 (1952).
Perdeck, A. C. Two types of orientation in migrating Sturnus vulgaris and Fringilla coelebs as revealed by displacement experiments. Ardea 46, 1–37 (1958).
Chernetsov, N., Kishkinev, D. & Mouritsen, H. A long-distance avian migrant compensates for longitudinal displacement during spring migration. Curr. Biol. 18, 188–190 (2008).
Chernetsov, N. et al. Migratory Eurasian reed warblers can use magnetic declination to solve the longitude problem. Curr. Biol. 27, 2647–2651.e2 (2017). This paper showed that adult, but not juvenile, Eurasian reed warblers can use magnetic declination—which requires two compasses—to correct for a virtual magnetic displacement from Kaliningrad to Scotland and therefore suggest that many bird species in Europe and North America could use magnetic declination to solve the enigmatic longitude problem.
Mouritsen, H. et al. An experimental displacement and over 50 years of tag-recoveries show that monarch butterflies are not true navigators. Proc. Natl Acad. Sci. USA 110, 7348–7353 (2013).
Lugo Ramos, J. S., Delmore, K. E. & Liedvogel, M. Candidate genes for migration do not distinguish migratory and non-migratory birds. J. Comp. Physiol. 203, 383–397 (2017).
Lohmann, K. J., Lohmann, C. M. F. & Putman, N. F. Magnetic maps in animals: nature’s GPS. J. Exp. Biol. 210, 3697–3705 (2007).
Mouritsen, H. & Mouritsen, O. A mathematical expectation model for bird navigation based on the clock-and-compass strategy. J. Theor. Biol. 207, 283–291 (2000).
Thorup, K. et al. Evidence for a navigational map stretching across the continental U.S. in a migratory songbird. Proc. Natl Acad. Sci. USA 104, 18115–18119 (2007).
Deutschlander, M. E., Phillips, J. B. & Munro, U. Age-dependent orientation to magnetically-simulated geographic displacements in migratory Australian silvereyes (Zosterops l. lateralis). Wilson J. Ornithol. 124, 467–477 (2012).
Holland, R. A. & Helm, B. A strong magnetic pulse affects the precision of departure direction of naturally migrating adult but not juvenile birds. J. R. Soc. Interface 10, 20121047 (2013).
Phillips, J. B., Freake, M. J., Fischer, J. H. & Borland, C. Behavioral titration of a magnetic map coordinate. J. Comp. Physiol. 188, 157–160 (2002).
Kishkinev, D., Chernetsov, N., Heyers, D. & Mouritsen, H. Migratory reed warblers need intact trigeminal nerves to correct for a 1,000 km eastward displacement. PLoS One 8, e65847 (2013).
Kishkinev, D., Chernetsov, N., Pakhomov, A., Heyers, D. & Mouritsen, H. Eurasian reed warblers compensate for virtual magnetic displacement. Curr. Biol. 25, R822–R824 (2015).
Gagliardo, A. Forty years of olfactory navigation in birds. J. Exp. Biol. 216, 2165–2171 (2013).
Geva-Sagiv, M., Las, L., Yovel, Y. & Ulanovsky, N. Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation. Nat. Rev. Neurosci. 16, 94–108 (2015).
Sarel, A., Finkelstein, A., Las, L. & Ulanovsky, N. Vectorial representation of spatial goals in the hippocampus of bats. Science 355, 176–180 (2017). This paper discovered a new type of spatial cell in the hippocampus of free-flying Egyptian fruit bats that is essential for navigational tasks—namely cells coding for the direction to a goal relative to an animal’s current heading.
Stalleicken, J. et al. Do monarch butterflies use polarized skylight for migratory orientation? J. Exp. Biol. 208, 2399–2408 (2005).
Heinze, S. & Reppert, S. M. Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69, 345–358 (2011).
Scholz, A. T., Horrall, R. M., Cooper, J. C. & Hasler, A. D. Imprinting to chemical cues: the basis for home stream selection in salmon. Science 192, 1247–1249 (1976).
DeBose, J. L. & Nevitt, G. A. The use of odors at different spatial scales: comparing birds with fish. J. Chem. Ecol. 34, 867–881 (2008).
Radford, C. A., Stanley, J. A., Simpson, S. D. & Jeffs, A. G. Juvenile coral reef fish use sound to locate habitats. Coral Reefs 30, 295–305 (2011).
Mouritsen, H. in Neurosciences—From Molecule to Behavior: A University Textbook (eds Galizia, C. G. & Lledo, P.-M.) 427–443 (Springer, Heidelberg, 2013)
Wiltschko, W. & Wiltschko, R. Magnetic compass of European robins. Science 176, 62–64 (1972).
Cochran, W. W., Mouritsen, H. & Wikelski, M. Migrating songbirds recalibrate their magnetic compass daily from twilight cues. Science 304, 405–408 (2004).
Lohmann, K. J. & Lohmann, C. A light-independent magnetic compass in the leatherback sea turtle. Biol. Bull. 185, 149–151 (1993).
Phillips, J. B. & Borland, S. C. Behavioral evidence for use of a light-dependent magnetoreception mechanism by a vertebrate. Nature 359, 142–144 (1992).
Dennis, T. E., Rayner, M. J. & Walker, M. M. Evidence that pigeons orient to geomagnetic intensity during homing. Proc. R. Soc. Lond. B 274, 1153–1158 (2007).
Guerra, P. A., Gegear, R. J. & Reppert, S. M. A magnetic compass aids monarch butterfly migration. Nat. Commun. 5, 4164 (2014).
Komolkin, A. V. et al. Theoretically possible spatial accuracy of geomagnetic maps used by migrating animals. J. R. Soc. Interface 14, 20161002 (2017).
Bazylinski, D. A. & Frankel, R. B. Magnetosome formation in prokaryotes. Nat. Rev. Microbiol. 2, 217–230 (2004).
Begall, S., Malkemper, E. P., Červený, J., Němec, P. & Burda, H. Magnetic alignment in mammals and other animals. Mamm. Biol. 78, 10–20 (2013).
Kirschvink, J. L., Winklhofer, M. & Walker, M. M. Biophysics of magnetic orientation: strengthening the interface between theory and experimental design. J. R. Soc. Interface 7, S179–S191 (2010).
Solov’yov, I., Hore, P. J., Ritz, T. & Schulten, K. in Quantum Effects in Biology 218–236 (Cambridge Univ. Press, Cambridge, 2014)
Meister, M. Physical limits to magnetogenetics. eLife 5, e17210 (2016).
Kattnig, D. R., Sowa, J. K., Solov’yov, I. A. & Hore, P. J. Electron spin relaxation can enhance the performance of a cryptochrome-based magnetic compass sensor. New J. Phys. 18, 063007 (2016).
Hore, P. J. & Mouritsen, H. The radical-pair mechanism of magnetoreception. Annu. Rev. Biophys. 45, 299–344 (2016). This tutorial review summarizes in detail all aspects of the radical-pair mechanism and the evidence for and against it as a magnetoreception mechanism, and aims to provide a must-read text for new scientists entering this field by explaining the biological aspects of the mechanism to physicists and chemists and the physicochemical and quantum mechanical aspects to biologists.
Winklhofer, M. & Mouritsen, H. A magnetic protein compass? Preprint at https://www.biorxiv.org/content/early/2016/12/15/094607 (2016).
Paulin, M. G. Electroreception and the compass sense of sharks. J. Theor. Biol. 174, 325–339 (1995).
Rosenblum, B., Jungerman, R. L. & Longfellow, L. in Magnetite Biomineralization and Magnetoreception in Organisms 223–232 (Plenum, New York, 1985)
Uebe, R. & Schüler, D. Magnetosome biogenesis in magnetotactic bacteria. Nat. Rev. Microbiol. 14, 621–637 (2016).
Winklhofer, M. & Kirschvink, J. L. A quantitative assessment of torque-transducer models for magnetoreception. J. R. Soc. Interface 7, S273–S289 (2010).
Shaw, J. et al. Magnetic particle-mediated magnetoreception. J. R. Soc. Interface 12, 20150499 (2015).
Treiber, C. D. et al. Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484, 367–370 (2012).
Mouritsen, H. Sensory biology: Search for the compass needles. Nature 484, 320–321 (2012).
Eder, S. H. et al. Magnetic characterization of isolated candidate vertebrate magnetoreceptor cells. Proc. Natl Acad. Sci. USA 109, 12022–12027 (2012).
Edelman, N. B. et al. No evidence for intracellular magnetite in putative vertebrate magnetoreceptors identified by magnetic screening. Proc. Natl Acad. Sci. USA 112, 262–267 (2015). This paper, together with Ref. 78, demonstrated that structures previously suggested to be strong candidates as magnetic-particle-based magnetoreceptors were dirt or non-magnetic iron accumulations, emphasizing that, to be considered as serious magnetoreception sensor candidates, magnetic particles must be proven to be located inside cells in exactly the same location and associated with nerve tissue in many individuals of the same species.
Walker, M. M. et al. Structure and function of the vertebrate magnetic sense. Nature 390, 371–376 (1997).
Fleissner, G. et al. Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 458, 350–360 (2003).
Wu, L.-Q. & Dickman, J. D. Neural correlates of a magnetic sense. Science 336, 1054–1057 (2012).
Němec, P., Altmann, J., Marhold, S., Burda, H. & Oelschläger, H. H. A. Neuroanatomy of magnetoreception: the superior colliculus involved in magnetic orientation in a mammal. Science 294, 366–368 (2001).
Burger, T. et al. Changing and shielded magnetic fields suppress c-Fos expression in the navigation circuit: input from the magnetosensory system contributes to the internal representation of space in a subterranean rodent. J. R. Soc. Interface 7, 1275–1292 (2010).
Johnsen, S. & Lohmann, K. J. The physics and neurobiology of magnetoreception. Nat. Rev. Neurosci. 6, 703–712 (2005).
Cadiou, H. & McNaughton, P. A. Avian magnetite-based magnetoreception: a physiologist’s perspective. J. R. Soc. Interface 7, S193–S205 (2010).
Stanley, S. A., Sauer, J., Kane, R. S., Dordick, J. S. & Friedman, J. M. Remote regulation of glucose homeostasis in mice using genetically encoded nanoparticles. Nat. Med. 21, 92–98 (2015).
Wheeler, M. A. et al. Genetically targeted magnetic control of the nervous system. Nat. Neurosci. 19, 756–761 (2016).
Qin, S. et al. A magnetic protein biocompass. Nat. Mater. 15, 217–226 (2016).
Schulten, K., Swenberg, C. E. & Weller, A. A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion. Z. Phys. Chem. 111, 1–5 (1978). This hardcore theoretical physics paper formulated the radical-pair hypothesis of magnetoreception for the first time, and it is now clear that it was decades ahead of its time.
Ritz, T., Adem, S. & Schulten, K. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707–718 (2000).
Maeda, K. et al. Chemical compass model of avian magnetoreception. Nature 453, 387–390 (2008). This paper proved that a radical-pair mechanism is fundamentally able to detect Earth-strength magnetic fields, as the authors synthesized a model compound in which they could directly observe that the photochemistry of a radical-pair mechanism was sensitive to Earth-strength magnetic fields.
Hiscock, H. G. et al. The quantum needle of the avian magnetic compass. Proc. Natl Acad. Sci. USA 113, 4634–4639 (2016).
Solov’yov, I. A., Mouritsen, H. & Schulten, K. Acuity of a cryptochrome and vision-based magnetoreception system in birds. Biophys. J. 99, 40–49 (2010).
Schwarze, S. et al. Migratory blackcaps can use their magnetic compass at 5 degrees inclination, but are completely random at 0 degrees inclination. Sci. Rep. 6, 33805 (2016).
Phillips, J. B., Deutschlander, M. E., Freake, M. J. & Borland, S. C. The role of extraocular photoreceptors in newt magnetic compass orientation: parallels between light-dependent magnetoreception and polarized light detection in vertebrates. J. Exp. Biol. 204, 2543–2552 (2001).
Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. Red light disrupts magnetic orientation of migratory birds. Nature 364, 525–527 (1993).
Schneider, T., Thalau, H. P., Semm, P. & Wiltschko, W. Melatonin is crucial for the migratory orientation of pied flycatchers Ficedula hypoleuca pallas. J. Exp. Biol. 194, 255–262 (1994).
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).
Ritz, T. et al. Magnetic compass of birds is based on a molecule with optimal directional sensitivity. Biophys. J. 96, 3451–3457 (2009).
Engels, S. et al. Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird. Nature 509, 353–356 (2014). This paper demonstrated in a massive series of reproducible, double-blinded experiments that anthropogenic electromagnetic fields in the low megahertz range and with an intensity 1,000 times lower than the current WHO guideline levels disrupt the magnetic compass sense of a night-migratory songbird; this strongly suggests that a quantum mechanical mechanism is responsible for magnetic compass sensing in these birds.
Kavokin, K. et al. Magnetic orientation of garden warblers (Sylvia borin) under 1.4 MHz radiofrequency magnetic field. J. R. Soc. Interface 11, 20140451 (2014).
Malkemper, E. P. et al. Magnetoreception in the wood mouse (Apodemus sylvaticus): influence of weak frequency-modulated radio frequency fields. Sci. Rep. 5, 9917 (2015).
Schwarze, S. et al. Weak broadband electromagnetic fields are more disruptive to magnetic compass orientation in a night-migratory songbird (Erithacus rubecula) than strong narrow-band fields. Front. Behav. Neurosci. 10, 55 (2016).
Hiscock, H. G., Mouritsen, H., Manolopoulos, D. E. & Hore, P. J. Disruption of magnetic compass orientation in migratory birds by radiofrequency electromagnetic fields. Biophys. J. 113, 1475–1484 (2017).
Björn, L. O. Photobiology: The Science of Light and Life (Springer, New York, 2015).
Liedvogel, M. et al. Chemical magnetoreception: bird cryptochrome 1a is excited by blue light and forms long-lived radical-pairs. PLoS One 2, e1106 (2007).
Maeda, K. et al. Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor. Proc. Natl Acad. Sci. USA 109, 4774–4779 (2012).
Mouritsen, H. et al. Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proc. Natl Acad. Sci. USA 101, 14294–14299 (2004).
Liedvogel, M. & Mouritsen, H. Cryptochromes—a potential magnetoreceptor: what do we know and what do we want to know? J. R. Soc. Interface 7, S147–S162 (2010).
Niessner, C. et al. Avian ultraviolet/violet cones identified as probable magnetoreceptors. PLoS One 6, e20091 (2011).
Nießner, C. et al. Seasonally changing cryptochrome 1b expression in the retinal ganglion cells of a migrating passerine bird. PLoS One 11, e0150377 (2016).
Bolte, P. et al. Localisation of the putative magnetoreceptive protein cryptochrome 1b in the retinae of migratory birds and homing pigeons. PLoS One 11, e0147819 (2016).
Günther, A. et al. Double-cone localization and seasonal expression pattern suggest a role in magnetoreception for European robin cryptochrome 4. Curr. Biol. 28, 211–223.e4 (2018). This paper suggests that cryptochrome 4 of night-migratory songbirds is a particularly strong candidate as the light-dependent magnetoreceptive protein because Cry4, in the retina, is exclusively expressed in the outer segments of the double cone and long-wavelength single cone photoreceptor cells, and is more strongly expressed in the migratory season in migratory birds, whereas no seasonal differences are observed in non-migratory birds.
Kutta, R. J., Archipowa, N., Johannissen, L. O., Jones, A. R. & Scrutton, N. S. Vertebrate cryptochromes are vestigial flavoproteins. Sci. Rep. 7, 44906 (2017).
Worster, S., Mouritsen, H. & Hore, P. J. A light-dependent magnetoreception mechanism insensitive to light intensity and polarization. J. R. Soc. Interface 14, 20170405 (2017).
Gegear, R. J., Casselman, A., Waddell, S. & Reppert, S. M. Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature 454, 1014–1018 (2008).
Fedele, G., Green, E. W., Rosato, E. & Kyriacou, C. P. An electromagnetic field disrupts negative geotaxis in Drosophila via a CRY-dependent pathway. Nat. Commun. 5, 4391 (2014).
Mouritsen, H., Feenders, G., Liedvogel, M., Wada, K. & Jarvis, E. D. Night-vision brain area in migratory songbirds. Proc. Natl Acad. Sci. USA 102, 8339–8344 (2005).
Heyers, D., Manns, M., Luksch, H., Güntürkün, O. & Mouritsen, H. A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLoS One 2, e937 (2007).
Zapka, M., Heyers, D., Liedvogel, M., Jarvis, E. D. & Mouritsen, H. Night-time neuronal activation of Cluster N in a day- and night-migrating songbird. Eur. J. Neurosci. 32, 619–624 (2010).
Zapka, M. et al. Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461, 1274–1277 (2009). This paper demonstrates that Cluster N processes light-dependent magnetic compass information in night-migratory songbirds, because Cluster N-lesioned birds could still use their sun and star compasses but not their magnetic compass, and because Cluster N is part of the thalamofugal visual pathway in night-migratory songbirds 129.
Wiltschko, W., Traudt, J., Güntürkün, O., Prior, H. & Wiltschko, R. Lateralization of magnetic compass orientation in a migratory bird. Nature 419, 467–470 (2002).
Hein, C. M., Engels, S., Kishkinev, D. & Mouritsen, H. Robins have a magnetic compass in both eyes. Nature 471, E11–E12 (2011).
Wiltschko, W., Traudt, J., Güntürkün, O., Prior, H. & Wiltschko, R. Wiltschko et al. reply. Nature 471, E12–E13 (2011).
Engels, S., Hein, C. M., Lefeldt, N., Prior, H. & Mouritsen, H. Night-migratory songbirds possess a magnetic compass in both eyes. PLOS One 7, e43271 (2012).
Heyers, D., Zapka, M., Hoffmeister, M., Wild, J. M. & Mouritsen, H. Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. Proc. Natl Acad. Sci. USA 107, 9394–9399 (2010).
Elbers, D., Bulte, M., Bairlein, F., Mouritsen, H. & Heyers, D. Magnetic activation in the brain of the migratory northern wheatear (Oenanthe oenanthe). J. Comp. Physiol. 203, 591–600 (2017).
Munro, U., Munro, J. A., Phillips, J. B., Wiltschko, R. & Wiltschko, W. Evidence for a magnetite-based navigational ‘map’ in birds. Naturwissenschaften 84, 26–28 (1997).
Wiltschko, W., Wiltschko, R. & Keeton, W. T. Effects of a ‘permanent’ clock-shift on the orientation of young homing pigeons. Behav. Ecol. Sociobiol. 1, 229–243 (1976).
Schmidt-Koenig, K., Ganzhorn, J. U. & Ranvaud, R. in Orientation in Birds 1–15 (Birkhäuser, Basel, 1991).
Emlen, S. T. The stellar-orientation system of a migratory bird. Sci. Am. 233, 102–111 (1975).
Heinze, S. & Homberg, U. Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315, 995–997 (2007).
Wiltschko, R., Walker, M. & Wiltschko, W. Sun-compass orientation in homing pigeons: compensation for different rates of change in azimuth? J. Exp. Biol. 203, 889–894 (2000).
Horváth, G. (Ed.) Polarized Light and Polarization Vision in Animal Sciences (Springer, Berlin, 2014).
Stalleicken, J., Labhart, T. & Mouritsen, H. Physiological characterization of the compound eye in monarch butterflies with focus on the dorsal rim area. J. Comp. Physiol. 192, 321–331 (2006).
Kamermans, M. & Hawryshyn, C. Teleost polarization vision: how it might work and what it might be good for. Phil. Trans. R. Soc. Lond. B 366, 742–756 (2011).
Wiltschko, W., Daum, P., Fergenbauer-Kimmel, A. & Wiltschko, R. The development of the star compass in garden warblers, Sylvia borin. Ethology 74, 285–292 (1987).
Michalik, A., Alert, B., Engels, S., Lefeldt, N. & Mouritsen, H. Star compass learning: how long does it take? J. Ornithol. 155, 225–234 (2014).
Mouritsen, H. & Larsen, O. N. Migrating songbirds tested in computer-controlled Emlen funnels use stellar cues for a time-independent compass. J. Exp. Biol. 204, 3855–3865 (2001).
Alert, B., Michalik, A., Helduser, S., Mouritsen, H. & Güntürkün, O. Perceptual strategies of pigeons to detect a rotational centre—a hint for star compass learning? PLoS One 10, e0119919 (2015).
Dacke, M., Baird, E., Byrne, M., Scholtz, C. H. & Warrant, E. J. Dung beetles use the Milky Way for orientation. Curr. Biol. 23, 298–300 (2013).
Zufall, F. & Munger, S. Chemosensory Transduction: The Detection of Odors, Tastes, and Other Chemostimuli (Academic, London, 2016).
Allison, J. D. & Cardé, R. T. Pheromone Communication in Moths: Evolution, Behavior, and Application (Univ. California Press, Oakland, 2016).
Jorge, P. E., Marques, P. A. & Phillips, J. B. Activational effects of odours on avian navigation. Proc. R. Soc. Lond. B 277, 45–49 (2010).
Wallraff, H. G. & Andreae, M. O. Spatial gradients in ratios of atmospheric trace gases: a study stimulated by experiments on bird navigation. Tellus B Chem. Phys. Meterol. 52, 1138–1157 (2000).
Kullberg, C., Henshaw, I., Jakobsson, S., Johansson, P. & Fransson, T. Fuelling decisions in migratory birds: geomagnetic cues override the seasonal effect. Proc. R. Soc. Lond. B 274, 2145–2151 (2007).
Schmitz, H. & Bleckmann, H. The photomechanic infrared receptor for the detection of forest fires in the beetle Melanophila acuminata (Coleoptera: Buprestidae). J. Comp. Physiol. A 182, 647–657 (1998).
Hagstrum, J. T. Infrasound and the avian navigational map. J. Exp. Biol. 203, 1103–1111 (2000).
Reynolds, A. M., Reynolds, D. R., Sane, S. P., Hu, G. & Chapman, J. W. Orientation in high-flying migrant insects in relation to flows: mechanisms and strategies. Phil. Trans. R. Soc. Lond. B 371, 20150392 (2016).
Sjöberg, S. & Muheim, R. A new view on an old debate: type of cue-conflict manipulation and availability of stars can explain the discrepancies between cue-calibration experiments with migratory songbirds. Front. Behav. Neurosci. 10, 29 (2016).
Åkesson, S. & Bianco, G. Route simulations, compass mechanisms and long-distance migration flights in birds. J. Comp. Physiol. A 203, 475–490 (2017).
Chernetsov, N., Kishkinev, D., Kosarev, V. & Bolshakov, C. V. Not all songbirds calibrate their magnetic compass from twilight cues: a telemetry study. J. Exp. Biol. 214, 2540–2543 (2011).
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B. & Moser, E. I. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801–806 (2005).
Cheeseman, J. F. et al. Way-finding in displaced clock-shifted bees proves bees use a cognitive map. Proc. Natl Acad. Sci. USA 111, 8949–8954 (2014).
I am grateful to many of the key scientists working in the field of animal navigation and magnetoreception, including all my colleagues and associated members of the proposed collaborative research centre SFB 1372, for inspiration and discussions, for commenting on earlier drafts of this manuscript, and for providing valuable input to various sections of the review. Funding was provided by the Air Force Office of Scientific Research (Air Force Material Command, USAF award no. FA9550-14-1-0095 and FA9550-14-1-0242), the DFG (Graduiertenkolleg 1885, SFB 1372), the ‘Ministerium für Wissenschaft und Kultur’ (Landesgraduiertenkolleg Nano-Energieforschung), and the University of Oldenburg.
Nature thanks S. Åkesson, J. Chapman and J. Phillips for their contribution to the peer review of this work.
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Mouritsen, H. Long-distance navigation and magnetoreception in migratory animals. Nature 558, 50–59 (2018). https://doi.org/10.1038/s41586-018-0176-1