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Tushar Tyagi Sanjay Kumar Bhardwaj

Abstract

The navigational systems of different animal species are by a wide margin less notable as compared to birds. Humans have been interested in how migratory birds discover their way more than thousands of miles for quite a long time. This review summarizes the cues and compass mechanisms applied in orientation and navigation by non-migrants, diurnal and nocturnal migrants. The magnetic compass, landmarks, olfactory, and memory of spatial cues en route were utilized in homing and migration. The equivalent is valid for the sun compass despite the fact that its job during migration might be undeniably less significant than commonly presumed. Stellar compass and celestial rotation, as a result of their nighttime accessibility, appear to influence the direction of nighttime migrants during the course of migration. The celestial cues go through notable changes because of the latitude shift during bird migration. Sunset cues alter their location with seasons and latitudes. The recognizable stars lose height and lastly vanish underneath the horizon, whereas new stars show up. These new ones must be calibrated. As celestial rotation not imparting a reference, it is not unexpected that the magnetic compass turns into the main cue that controls the directional importance of stars and sunset cues. Field studies have revealed that, in certain species, a considerable extent of individuals get back to similar breeding, overwintering, and stopover areas in progressive years. This review proposes that migratory birds have advanced uncommon cognitive capacities that empower them to achieve these accomplishments.      

Article Details

Article Details

Keywords

Birds, Compass mechanisms, Cues, Navigation, Orientation

References
Able, K. P. (2001). The concepts and terminology of bird navigation. Journal of Avian Biology, 32(2), 174–183. https://doi.org/10.1034/j.1600-048X.2001.320211.x
Able, K. P. & Able, M. A. (1993). Daytime calibration of magnetic orientation in a migratory bird requires a view of skylight polarization. Nature, 364(6437), 523–525. https://doi.org/10.1038/364523a0
Able, K. P. & Able, M. A. (1995). Interactions in the flexible orientation system of a migratory bird. Nature, 375(6528), 230–232. https://doi.org/10.1038/375230a0
Able, K. P. & Able, M. A. (1996). Migratory orientation: Autumn calibration of magnetic orientation is not evident in spring. Naturwissenschaften, 83, 517–518. https://doi.org/10.1007/BF01141954
Able, K. P. & Cherry, J. D. (1986). Mechanisms of dusk orientation in white-throated sparrows (Zonotrichia albicollis): Clock-shift experiments. Journal of Comparative Physiology A, 159(1), 107–113. https://doi.org/10.1007/BF00612501
Able, K. P. & Dillon, P. M. (1977). Sun Compass Orientation in a Nocturnal Migrant, the White-Throated Sparrow. The Condor, 79(3), 393–395. https://doi.org/10.2307/136 8027
Able, K.P. (1982). Skylight polarization patterns at dusk influence migratory orientation in birds. Nature, 299(5883), 550–551. https://doi.org/10.1038/299550a0
Åkesson, S., Odin, C., Hegedus, R., Ilieva, M., Sjoholm, C., Farkas, A. & Horvath, G. (2015). Testing avian compass calibration: Comparative experiments with diurnal and nocturnal passerine migrants in South Sweden. Biology Open, 4(1), 35–47. https://doi.org/10.1242/bio.201498 37
Åkesson, S., Jonzén, N., Pettersson, J., Rundberg, M. & Sandberg, R. (2006). Effects of magnetic manipulations on orientation: Comparing diurnal and nocturnal passerine migrants on Capri, Italy in autumn. Ornis Svecica, 16, 55–61.
Alerstam, T., Chapman, J. W., Bäckman, J., Smith, A. D., Karlsson, H., Nilsson, C., Reynolds, D. R., Klaassen, R. H. G. & Hill, J. K. (2011). Convergent patterns of long-distance nocturnal migration in noctuid moths and passerine birds. Proceedings of the Royal Society B: Biological Sciences, 278(1721), 3074–3080. https://doi.org/10.1098/rspb.2011.0058
Alert, B., Michalik, A., Helduser, S., Mouritsen, H. & Güntürkün, O. (2015). Perceptual Strategies of Pigeons to Detect a Rotational Centre—A Hint for Star Compass Learning? PLOS ONE, 10(3), e0119919. https://doi.org/10.1371/ journal.pone.0119919
Bellono, N. W., Leitch, D. B. & Julius, D. (2018). Molecular tuning of electroreception in sharks and skates. Nature, 558(7708), 122–126. https://doi.org/10.1038/s41586-018-0160-9
Bellrose, F. C. (1972). Possible steps in the evolutionary development of birds’ navigation. In S. R. Galler, K. Schmidt-Koenig, G. J. Jacobs & R. E. Belleville (Eds.), Animal Orientation and Navigation: Vol. NASA SP-262 (pp. 223–258). US Government Printing Office.
Benvenuti, S. & Fiaschi, V. (1983). Pigeon homing: Combined effect of olfactory deprivation and visual impairment. Comparative Biochemistry and Physiology Part A: Physiology, 76(4), 719–723. https://doi.org/10.1016/0300-9629(83)90133-0
Berthold, P. (1999). A comprehensive theory for the evolution, control and adaptability of avian migration. Ostrich, 70(1), 1–11. https://doi.org/10.1080/00306525.1999.963 9744
Bingman, V. P. (1987). Earth’s Magnetism and the Nocturnal Orientation of Migratory European Robins. The Auk, 104(3), 523–525. https://doi.org/10.2307/4087555
Bingman, V. P. & Wiltschko, W. (1988). Orientation of Dunnocks (Prunella modularis) at Sunset. Ethology, 77(1), 1–9. https://doi.org/10.1111/j.1439-0310.1988.tb00187.x
Bonadonna, F., Bajzak, C., Benhamou, S., Igloi, K., Jouventin, P., Lipp, H. P. & Dell’Omo, G. (2005). Orientation in the wandering albatross: Interfering with magnetic perception does not affect orientation performance. Proceedings of the Royal Society B: Biological Sciences, 272(1562), 489–495. https://doi.org/10.1098/rspb.2004.2984
Boström, J. E., Åkesson, S. & Alerstam, T. (2012). Where on earth can animals use a geomagnetic bi-coordinate map for navigation? Ecography, 35(11), 1039–1047. https://doi.org/10.1111/j.1600-0587.2012.07507.x
Bridge, E., Kelly, J., Contina, A., Gabrielson, R., MacCurdy, R. & Winkler, D. (2013). Advances in tracking small migratory birds: A technical review of light-level geolocation. Journal of Field Ornithology, 84, 121–137. https://doi.org/10.1111 /jofo.12011
Brines, M. L. & Gould, J. L. (1982). Skylight Polarization patterns and Animal Orientation. Journal of Experimental Biology, 96(1), 69–91.
Chaves, I., Pokorny, R., Byrdin, M., Hoang, N., Ritz, T., Brettel, K., Essen, L.-O., van der Horst, G. T. J., Batschauer, A. & Ahmad, M. (2011). The Cryptochromes: Blue Light Photoreceptors in Plants and Animals. Annual Review of Plant Biology, 62(1), 335–364. https://doi.org/10.1146/annurev-arplant-042110-103759
Chernetsov, N. (2015). Avian compass systems: Do all migratory species possess all three? Journal of Avian Biology, 46(4), 342–343. https://doi.org/10.1111/jav.00593
Chernetsov, N., Kishkinev, D., Kosarev, V. & Bolshakov, C. V. (2011). Not all songbirds calibrate their magnetic compass from twilight cues: A telemetry study. Journal of Experimental Biology, 214(15), 2540–2543. https://doi.org/10.1242/ jeb.057729
Chernetsov, N., Kishkinev, D. & Mouritsen, H. (2008). A Long-Distance Avian Migrant Compensates for Longitudinal Displacement during Spring Migration. Current Biology, 18(3), 188–190. https://doi.org/10.1016/j.cub.2008.0 1.018
Chernetsov, N., Pakhomov, A., Davydov, A., Cellarius, F. & Mouritsen, H. (2020). No evidence for the use of magnetic declination for migratory navigation in two songbird species. PLOS ONE, 15(4), e0232136. https://doi.org/10.1371/journal.pone. 0232136
Chernetsov, N., Pakhomov, A., Kobylkov, D., Kishkinev, D., Holland, R. A. & Mouritsen, H. (2017). Migratory Eurasian Reed Warblers Can Use Magnetic Declination to Solve the Longitude Problem. Current Biology, 27(17), 2647-2651.e2. https://doi.org/10.1016/j.cub.2017.07.024
Cochran, W. W., Mouritsen, H. & Wikelski, M. (2004). Migrating Songbirds Recalibrate Their Magnetic Compass Daily from Twilight Cues. Science, 304(5669), 405–408. https://doi.org/10.1126/science.1095844
Cronin, T. W., Warrant, E. J. & Greiner, B. (2006). Celestial polarization patterns during twilight. Applied Optics, 45(22), 5582–5589. https://doi.org/10.1364/ AO.45.005582
Dennis, T. E., Rayner, M. J. & Walker, M. M. (2007). Evidence that pigeons orient to geomagnetic intensity during homing. Proceedings of the Royal Society B: Biological Sciences, 274(1614), 1153–1158. https://doi.org/10.1098/rspb.2007.3768
Duff, S. J., Brownlie, L. A., Sherry, D. F. & Sangster, M. (1998). Sun compass and landmark orientation by black-capped chickadees (Parus atricapillus). Journal of Experimental Psychology: Animal Behavior Processes, 24(3), 243–253. https://doi.org/10.1037/0097-7403.24.3.243
Egevang, C., Stenhouse, I. J., Phillips, R. A., Petersen, A., Fox, J. W. & Silk, J. R. D. (2010). Tracking of Arctic terns Sterna paradisaea reveals longest animal migration. Proceedings of the National Academy of Sciences of the United States of America, 107(5), 2078–2081. https://doi.org/1 0.1073/pnas.0909493107
Emlen, S. T. (1967a). Migratory Orientation in the Indigo Bunting, Passerina cyanea: Part I: Evidence for Use of Celestial Cues. The Auk, 84(3), 309–342. https://doi.org/10.2307/4083084
Emlen, S. T. (1967b). Migratory Orientation in the Indigo Bunting, Passerina cyanea. Part II: Mechanism of Celestial Orientation. The Auk, 84(4), 463–489. https://doi.org/10.2307/4083330
Emlen, S. T. (1969a). Bird Migration: Influence of Physiological State upon Celestial Orientation. Science, 165(3894), 716–718. https://doi.org/10.1126/science.165.389 4.716
Emlen, S. T. (1969b). The development of migratory orientation in young indigo bunting, Passerina cyanea. Living Bird, 8, 115-126.
Emlen, S. T. (1970). Celestial Rotation: Its Importance in the Development of Migratory Orientation. Science, 170(3963), 1198–1201. https://doi.org/10.1126/ science.170.3 963.1198
Emlen, S. T. (1975a). The stellar-orientation system of a migratory bird. Scientific American, 233(2), 102–111. https://doi.org/10.1038/scientificamerican0875-102
Emlen, S. T. (1975b). Migration: Orientation and Navigation. In D. S. Farner & J. R. King (Eds.), Avian Biology: Vol. V (pp. 129–219). London: Academic Press.
Falkenberg, G., Fleissner, G., Schuchardt, K., Kuehbacher, M., Thalau, P., Mouritsen, H., Heyers, D., Wellenreuther, G. & Fleissner, G. (2010). Avian Magnetoreception: Elaborate Iron Mineral Containing Dendrites in the Upper Beak Seem to Be a Common Feature of Birds. PLoS ONE, 5(2), e9231. https://doi.org/10.1371/journal.pone.0009231
Freire, R., Munro, U. H., Rogers, L. J., Wiltschko, R. & Wiltschko, W. (2005). Chickens orient using a magnetic compass. Current Biology: CB, 15(16), R620-621. https://doi.org/10.1016/j.cub.2005.08.017
Gagliardo, A. (2013). Forty years of olfactory navigation in birds. Journal of Experimental Biology, 216(12), 2165–2171. https://doi.org/10.1242/jeb.070250
Gagliardo, A., Bried, J., Lambardi, P., Luschi, P., Wikelski, M. & Bonadonna, F. (2013). Oceanic navigation in Cory’s shearwaters: Evidence for a crucial role of olfactory cues for homing after displacement. Journal of Experimental Biology, 216(15), 2798–2805. https://doi.org/10.1242/jeb.085738
Gagliardo, A., Ioalè, P., Filannino, C. & Wikelski, M. (2011). Homing Pigeons Only Navigate in Air with Intact Environmental Odours: A Test of the Olfactory Activation Hypothesis with GPS Data Loggers. PLoS ONE, 6(8), e22385. https://doi.org/10.1371/journal.pone.0022385
Gagliardo, A., Savini, M., De Santis, A., Dell’Omo, G. & Ioalè, P. (2009). Re-orientation in clock-shifted homing pigeons subjected to a magnetic disturbance: A study with GPS data loggers. Behavioral Ecology and Sociobiology, 64(2), 289–296. https://doi.org/10.1007/s00265-009-0847-x
Grifn, D. R. (1952). Bird navigation. Biol. Rev. Camb. Philos. Soc., 27, 359–400.
Guilford, T. & de Perera, T. B. (2017). An associative account of avian navigation. Journal of Avian Biology, 48(1), 191–195. https://doi.org/10.1111/jav.01355
Günther, A., Einwich, A., Sjulstok, E., Feederle, R., Bolte, P., Koch, K.-W., Solov’yov, I. A. & Mouritsen, H. (2018). Double-Cone Localization and Seasonal Expression Pattern Suggest a Role in Magnetoreception for European Robin Cryptochrome 4. Current Biology: CB, 28(2), 211-223.e4. https://doi.org/10.1016/j.cub.2017.12.003
Healy, S. D., Clayton, N. S. & Krebs, J. R. (1994). Development of hippocampal specialisation in two species of tit (Parus spp.). Behavioural Brain Research, 61(1), 23–28. https://doi.org/10.1016/0166-4328(94)90004-3
Healy, S. D., Gwinner, E. & Krebs, J. R. (1996). Hippocampal volume in migratory and non-migratory warblers: Effects of age and experience. Behavioural Brain Research, 81(1–2), 61–68. https://doi.org/10.1016/S0166-4328(96)00044-7
Helbig, A. J. & Wiltschko, W. (1989). The skylight polarization patterns at dusk affect the orientation behavior of blackcaps, Sylvia atricapilla. The Science of Nature, 76(5), 227–229. https://doi.org/10.1007/BF00627697
Helbig, A. J. (1990). Are orientation mechanisms among migratory birds speciesospecific? Trends in Ecology and Evolution, 5(11), 365–367. https://doi.org/10.1016/0169-5347(90)90096-V
Helbig, A. J. (1991). Dusk orientation of migratory european robins, Erithacus rubecula: The role of sun-related directional information. Animal Behaviour, 41(2), 313–322. https://doi.org/10.1016/S0003-3472(05)80483-X
Helbig, A. J., Orth, G., Laske, V. & Wiltschko, W. (1987). Migratory Orientation and Activity of the Meadow Pipit (Anthus pratensis): A Comparative Observational and Experimental Field Study. Behaviour, 103(4), 276–293.
Heyers, D., Zapka, M., Hoffmeister, M., Wild, J. M. & Mouritsen, H. (2010). Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. Proceedings of the National Academy of Sciences, 107(20), 9394–9399. https://doi.org/10.1073/pnas.0907068107
Hoffmann, K. (1954). Versuche zu der im Richtungsfinden der Vögel enthaltenen Zeitschätzung. [Experiments on the time sense used in direction-finding by birds.]. Zeitschrift Für Tierpsychologie, 11, 453–475. https://doi.org/10.1111/j.1439-0310.1954.tb02169.x
Holland, R. A. (2014). True navigation in birds: From quantum physics to global migration: Bird navigation. Journal of Zoology, 293(1), 1–15. https://doi.org/10.1111/jzo.12107
Holland, R. A., Thorup, K., Gagliardo, A., Bisson, I. A., Knecht, E., Mizrahi, D. & Wikelski, M. (2009). Testing the role of sensory systems in the migratory heading of a songbird. Journal of Experimental Biology, 212(24), 4065–4071. https://doi.org/10.1242/jeb.034504
Hore, P. J. & Mouritsen, H. (2016). The Radical-Pair Mechanism of Magnetoreception. Annual Review of Biophysics, 45(1), 299–344. https://doi.org/10.1146/annurev-biophys-032116-094545
Horváth, G. (2014). Polarized Light and Polarization Vision in Animal Sciences. Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-642-54718-8
Horváth, G., Barta, A. & Hegedüs, R. (2014). Polarization of the Sky. In G. Horváth (Ed.), Polarized Light and Polarization Vision in Animal Sciences (pp. 367–406). Springer Berlin Heidelberg.
Jorge, P. E., Marques, A. E. & Phillips, J. B. (2009). Activational Rather Than Navigational Effects of Odors on Homing of Young Pigeons. Current Biology, 19(8), 650–654. https://doi.org/10.1016/j.cub.2009.02.066
Jorge, P. E., Marques, P. A. M. & Phillips, J. B. (2010). Activational effects of odours on avian navigation. Proceedings of the Royal Society B: Biological Sciences, 277(1678), 45–49. https://doi.org/10.1098/rspb.2009.1521
Katz, Y. B. (1985). Sunset and the orientation of European robins (Erithacus rubecula). Animal Behaviour, 33(3), 825–828. https://doi.org/10.1016/S0003-3472(85)80016-6
Katz, Y. & Michelsons, H. (1978). Influence of direction altering of stellar or magnetic meridians on orientation of European Robins in circular cages at planetarium. In H. Mihelsons, P. Blüm & J. Baumaris, Orientazija Ptiz (Orientierung der Vögel) (pp. 180–193). Riga: Zinatne.
Keeton, W. T. (1979). Avian Orientation and Navigation. Annual Review of Physiology, 41(1), 353–366. https://doi.org/10.1146/annurev.ph.41.030179.002033
Kishkinev, D. (2015). Sensory mechanisms of long-distance navigation in birds: A recent advance in the context of previous studies. Journal of Ornithology, 156(1), 145–161. https://doi.org/10.1007/s10336-015-1215-4
Kishkinev, D., Chernetsov, N., Heyers, D. & Mouritsen, H. (2013). Migratory Reed Warblers Need Intact Trigeminal Nerves to Correct for a 1,000 km Eastward Displacement. PLOS ONE, 8(6), e65847. https://doi.org/10.1371/journal.pone.0065847
Kishkinev, D., Packmor, F., Zechmeister, T., Winkler, H.-C., Chernetsov, N., Mouritsen, H. & Holland, R. A. (2021). Navigation by extrapolation of geomagnetic cues in a migratory songbird. Current Biology, S096 0982 221001160. https://doi.org/10.1016/j.cub.2021.01.0 51
Kramer, G. (1949). Über Richtungstendenzen bei der nächtlichen Zugunruhe gekäfigter Vögel. In E. Mayr & E. Schüz (Eds.), Ornithologie als biologische Wissenschaft (pp. 269–283). Heidelberg.
Kramer, G. (1950). Weitere Analyse der Faktoren, welche die Zugaktivität des gekäfigten Vogels orientieren. Naturwissenschaften, 37(16), 377–378. https://doi.org/10.1007/BF00626007
Kullberg, C., Henshaw, I., Jakobsson, S., Johansson, P. & Fransson, T. (2007). Fuelling decisions in migratory birds: Geomagnetic cues override the seasonal effect. Proceedings of the Royal Society B: Biological Sciences, 274(1622), 2145–2151. https://doi.org/10.1098/rspb.2007.0 554
Maeda, K., Henbest, K. B., Cintolesi, F., Kuprov, I., Rodgers, C. T., Liddell, P. A., Gust, D., Timmel, C. R. & Hore, P. J. (2008). Chemical compass model of avian magnetoreception. Nature, 453(7193), 387–390. https://doi.org/1 0.1038/nature06834
Matthews, G. V. T. (1951). The Experimental Investigation of Navigation in Homing Pigeons. Journal of Experimental Biology, 28(4), 508–536.
Matthews, G. V. T. (1963). The astronomical basis of “nonsense” orientation. Proc. XIIIth Internat. Ornithol. Congr., Ithaca, N.Y., 1962, 415–429.
Merkel, F. W. & Wiltschko, W. (1965). Magnetismus und Richtungsfinden zugunruhiger Rotkehlchen (Erithacus rubecula). 71–77.
Mettke-Hofmann, C. & Gwinner, E. (2003). Long-term memory for a life on the move. Proceedings of the National Academy of Sciences, 100(10), 5863–5866. https://doi.org/10.1073/pnas.1037505100
Michalik, A., Alert, B., Engels, S., Lefeldt, N. & Mouritsen, H. (2014). Star compass learning: How long does it take? Journal of Ornithology, 155(1), 225–234. https://doi.org/10.1007/s10336-013-1004-x
Middendorf, A. T. von. (1855). Die Isepiptesen Russlands. Grundlagen zur Erforschung der Zugzeiten und Zugrichtungen der Vögel Russlands. Buchdruckerei der K. Akademie der Wissenschaften.
Moore, F. R. (1978). Sunset and the orientation of a nocturnal migrant bird. Nature, 274(5667), 154–156. https://doi.org/10.1038/274154a0
Moore, F. R. (1982). Sunset and the orientation of a nocturnal bird migrant: A mirror experiment. Behavioral Ecology and Sociobiology, 10(2), 153–155. https://doi.org/10.1 007/BF00300176
Moore, F. R. (1986). Sunrise, Skylight Polarization, and the Early Morning Orientation of Night-Migrating Warblers. The Condor, 88(4), 493–498. https://doi.org/10.2307/1 368277
Moore, F. R. (1987). Sunset and the Orientation Behaviour of Migrating Birds. Biological Reviews, 62(1), 65–86. https://doi.org/10.1111/j.1469-185X.1987.tb00626.x
Moore, F. R. & Phillips, J. B. (1988). Sunset, skylight polarization and the migratory orientation of yellow-rumped warblers, Dendroica coronata. Animal Behaviour, 36(6), 1770–1778. https://doi.org/10.1016/S0003-3472(88)80116-7
Mouritsen, H. (2003a). Spatiotemporal Orientation Strategies of Long-Distance Migrants. In P. Berthold, E. Gwinner & E. Sonnenschein (Eds.), Avian Migration (pp. 493–513). Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-662-05957-9_34
Mouritsen, H. (2003b). Waved albatrosses can navigate with strong magnets attached to their head. Journal of Experimental Biology, 206(22), 4155–4166. https://doi.org/10.1242/jeb.00650
Mouritsen, H. (2013). The Magnetic Senses. In C. Galizia & P. Lledo (Eds.), Neurosciences—From Molecule to Behavior: A university textbook (pp. 427–443). Springer.
Mouritsen, H. (2015). Sturkie’s Avian Physiology (C. Scanes, Ed.). Elsevier.
Mouritsen, H. (2018). Long-distance navigation and magnetoreception in migratory animals. Nature, 558(7708), 50–59. https://doi.org/10.1038/s41586-018-0176-1
Mouritsen, H., Feenders, G., Liedvogel, M., Wada, K. & Jarvis, E. D. (2005). Night-vision brain area in migratory songbirds. Proceedings of the National Academy of Sciences, 102(23), 8339–8344. https://doi.org/10.1073/pnas.0409575102
Mouritsen, H., Heyers, D. & Güntürkün, O. (2016). The Neural Basis of Long-Distance Navigation in Birds. Annual Review of Physiology, 78(1), 133–154. https://doi.org/1 0.1146/annurev-physiol-021115-105054
Muheim, R. (2011). Behavioural and physiological mechanisms of polarized light sensitivity in birds. Philosophical Transactions of the Royal Society B: Biological Sciences, 366(1565), 763–771. https://doi.org/10.1098/rstb.20 10.0196
Muheim, R., Åkesson, S. & Alerstam, T. (2003). Compass orientation and possible migration routes of passerine birds at high arctic latitudes. Oikos, 103(2), 341–349. https://doi.org/10.1034/j.1600-0706.2003.12122.x
Muheim, R., Åkesson, S. & Phillips, J. B. (2007). Magnetic compass of migratory Savannah sparrows is calibrated by skylight polarization at sunrise and sunset. Journal of Ornithology, 148(2), 485–494. https://doi.org/10.1007/s10336-007-0187-4
Muheim, R., Bäckman, J. & Åkesson, S. (2002). Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light. Journal of Experimental Biology, 205(24), 3845–3856.
Muheim, R., Moore, F. R. & Phillips, J. B. (2006a). Calibration of magnetic and celestial compass cues in migratory birds—A review of cue-conflict experiments. Journal of Experimental Biology, 209(1), 2–17. https://doi.org/10.1242/jeb.01960
Muheim, R., Phillips, J. B. & Åkesson, S. (2006b). Polarized Light Cues Underlie Compass Calibration in Migratory Songbirds. Science, 313(5788), 837–839. https://doi.org/10.1126/science.1129709
Muheim, R., Phillips, J. B. & Deutschlander, M. E. (2009). White-throated sparrows calibrate their magnetic compass by polarized light cues during both autumn and spring migration. Journal of Experimental Biology, 212(21), 3466–3472. https://doi.org/10.1242/jeb.032771
Muheim, R., Sjöberg, S. & Pinzon-Rodriguez, A. (2016). Polarized light modulates light-dependent magnetic compass orientation in birds. Proceedings of the National Academy of Sciences, 113(6), 1654–1659. https://doi.org/10.1073/pnas.1513391113
Munro, U. & Wiltschko, W. (1993a). Magnetic compass orientation in the yellow-faced honeyeater, Lichenostomus chrysops, a day migrating bird from Australia. Behavioral Ecology and Sociobiology, 32(2), 141–145. https://doi.org/10.1007/ BF00164047
Munro, U. & Wiltschko, R. (1993b). Clock-Shift Experiments with Migratory Yellow- Faced Honeyeaters, Lichenostomus Chrysops (meliphagidae), an Australian Day-Migrating Bird. Journal of Experimental Biology, 181(1), 233–244.
Munro, U. & Wiltschko, R. (1995). The role of skylight polarization in the orientation of a day-migrating bird species. Journal of Comparative Physiology A, 177(3). https://doi.org/10.1007/BF00192424
National Centers for Environmental Information. (2020). Maps of magnetic elements from the WMM2020. https://www.ngdc.noaa.gov/geomag/WMM/image.shtml
Nimpf, S., Nordmann, G. C., Kagerbauer, D., Malkemper, E. P., Landler, L., Papadaki-Anastasopoulou, A., Ushakova, L., Wenninger-Weinzierl, A., Novatchkova, M., Vincent, P., Lendl, T., Colombini, M., Mason, M. J. & Keays, D. A. (2019). A Putative Mechanism for Magnetoreception by Electromagnetic Induction in the Pigeon Inner Ear. Current Biology, 29(23), 4052-4059.e4. https://doi.org/10.1016/j.cub. 2019.09.048
Pakhomov, A. & Chernetsov, N. (2014). Early evening activity of migratory Garden Warbler Sylvia borin: Compass calibration activity? Journal of Ornithology, 155(3), 621–630. https://doi.org/10.1007/s10336-014-1044-x
Papi, F., Fiore, L., Fiaschi, V. & Benvenuti, S. (1971). The Influence of Olfactory Nerve Section on the Homing Capacity of Carrier Pigeons. Monitore Zoologico Italiano - Italian Journal of Zoology, 5(4), 265–267. https://doi.org/10.1080/00269786. 1971.10736180
Phillips, J. B. & Moore, F. R. (1992). Calibration of the sun compass by sunset polarized light patterns in a migratory bird. Behavioral Ecology and Sociobiology, 31(3), 189–193. https://doi.org/10.1007/BF00168646
Pinzon-Rodriguez, A. & Muheim, R. (2017). Zebra finches have a light-dependent magnetic compass similar to migratory birds. Journal of Experimental Biology, 220(7), 1202–1209. https://doi.org/10.1242/jeb.148098
Pollonara, E., Luschi, P., Guilford, T., Wikelski, M., Bonadonna, F. & Gagliardo, A. (2015). Olfaction and topography, but not magnetic cues, control navigation in a pelagic seabird: Displacements with shearwaters in the Mediterranean Sea. Scientific Reports, 5(1), 16486. https://doi.org/10.1038/srep16486
Qin, S., Yin, H., Yang, C., Dou, Y., Liu, Z., Zhang, P., Yu, H., Huang, Y., Feng, J., Hao, J., Hao, J., Deng, L., Yan, X., Dong, X., Zhao, Z., Jiang, T., Wang, H.-W., Luo, S.-J. & Xie, C. (2016). A magnetic protein biocompass. Nature Materials, 15(2), 217–226. https://doi.org/10.1038/nmat4484
Ramos, J. S. L., Delmore, K. E. & Liedvogel, M. (2017). Candidate genes for migration do not distinguish migratory and non-migratory birds. Journal of Comparative Physiology A, 203(6), 383–397. https://doi.org/10.1007/s00359-017-1184-6
Rappl, R., Wiltschko, R., Weindler, P., Berthold, P. & Wiltschko, W. (2000). Orientation Behavior of Garden Warblers (Sylvia borin) Under Monochromatic Light of Various Wavelengths. The Auk, 117, 256–260. https://doi.org/10.1642/0004-8038(2000)117[0256:OBOGWS]2.0.CO;2
Reboreda, J. C., Clayton, N. S. & Kacelnik, A. (1996). Species and sex differences in hippocampus size in parasitic and non-parasitic cowbirds. Neuroreport, 7(2), 505–508. https://doi.org/10.1097/00001756-199601310-00031
Ritz, T., Adem, S. & Schulten, K. (2000). A Model for Photoreceptor-Based Magnetoreception in Birds. Biophysical Journal, 78(2), 707–718. https://doi.org/10.1016/S0006-3495(00)76629-X
Ritz, T., Wiltschko, R., Hore, P. J., Rodgers, C. T., Stapput, K., Thalau, P., Timmel, C. R. & Wiltschko, W. (2009). Magnetic Compass of Birds Is Based on a Molecule with Optimal Directional Sensitivity. Biophysical Journal, 96(8), 3451–3457. https://doi.org/10.1016/j.bpj.2008.11.072
Roberts, N. W., Porter, M. L. & Cronin, T. W. (2011). The molecular basis of mechanisms underlying polarization vision. Philosophical Transactions of the Royal Society B: Biological Sciences, 366(1565), 627–637. https://doi.org/10.1098/rstb. 2010.0206
Salewski, V., Bairlein, F. & Leisler, B. (2000). Recurrence of some palaearctic migrant passerine species in West Africa. Ringing and Migration, 20(1), 29–30. https://doi.org/10.1080/03078698.2000.9674224
Sandberg, R., Bäckman, J., Moore, F. R. & Lõhmus, M. (2000). Magnetic information calibrates celestial cues during migration. Animal Behaviour, 60(4), 453–462. https://doi.org/10.1006/anbe.2000.1582
Sandberg, R., Ottosson, U. & Pettersson, J. (1991). Magnetic orientation of migratory wheatears (Oenanthe oenanthe) in Sweden and Greenland. Journal of Experimental Biology, 155(1), 51–64.
Sauer, F. (1957). Die Sternenorientierung nächtlich ziehender Grasmücken (Sylvia atricapilla, borin und curruca). Zeitschrift Für Tierpsychologie, 14(1), 20–70. https://doi.org/10.1111/j.1439-0310.1957.tb00525.x
Schiffner, I., Siegmund, B. & Wiltschko, R. (2014). Following the sun: A mathematical analysis of the tracks of clock-shifted homing pigeons. Journal of Experimental Biology, 217(15), 2643–2649. https://doi.org/10.1242/jeb.104182
Schlichte, H.-J. (1973). Untersuchungen über die Bedeutung optischer Parameter für das Heimkehrverhalten der Brieftaube. Zeitschrift Für Tierpsychologie, 32(3), 257–280. https://doi.org/10.1111/j.1439-0310.197 3.tb01105.x
Schmaljohann, H., Fox, J. & Bairlein, F. (2012). Phenotypic response to environmental cues, orientation and migration costs in songbirds flying halfway around the world. Animal Behaviour, 84, 623–640. https://doi.org/10.1016/j.anbehav.2012.06.018
Schmidt-Koenig, K. (1972). New experiments on the effect of clock-shifts on homing in pigeons. In S. R. Galler, K. Schmidt-Koenig, G. J. Jacobs & R. E. Belleville (Eds.), Animal Orientation and Navigation: Vol. NASA SP-262 (pp. 275–282). US Government Printing Office.
Sjöberg, S. & Muheim, R. (2016). 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. Frontiers in Behavioral Neuroscience, 10. https://doi.org/10.3389/fnbeh.2016.00029
Skiles, D. D. (1985). The geomagnetic field Its nature, history, and biological relevance. In J. L. Kirschvink, D. S. Jones & B. J. MacFadden (Eds.), Magnetite Biomineralization and Magnetoreception in Organisms (Vol. 5, pp. 43–102). Springer US. https://doi.org/10.1007/978-1-4613-0313-8_3
Tyagi, T. & Bhardwaj, S. K. (2021). Magnetic compass orientation in a palaearctic-Indian night migrant, The redheaded bunting. Animals, 11(6), 1541. https://doi.o rg/10.3390/ani11061541
Viguier, C. (1882). Le sens de l’orientation et ses organes chez les animaux et chez l’homme. Revue Philosophique de La France et de l’Etranger, 1–36.
Volman, S. F., Grubb, Jr., T. C. & Schuett, K. C. (1997). Relative Hippocampal Volume in Relation to Food-Storing Behavior in Four Species of Woodpeckers. Brain, Behavior and Evolution, 49(2), 110–120. https://doi.org/10.1159/000112985
Voss, J., Keary, N. & Bischof, H.-J. (2007). The use of the geomagnetic field for short distance orientation in zebra finches. Neuroreport, 18(10), 1053–1057. https://doi.org/10.1097/WNR.0b013e32818b2a21
Wiltschko, R., Nohr, D. & Wiltschko, W. (1981). Pigeons with a deficient sun compass use the magnetic compass. Science (New York, N.Y.), 214(4518), 343–345. https://doi.org/10.1126/science.7280697
Wiltschko, R., Walker, M. & Wiltschko, W. (2000). Sun-compass orientation in homing pigeons: Compensation for different rates of change in azimuth? The Journal of Experimental Biology, 203(Pt 5), 889–894.
Wiltschko, R. (1981). Die Sonnenorientierung der Vögel. II. Entwicklung des Sonnenkompaß und sein Stellenwert im Orientierungssystem. Journal of Ornithology, 122(1), 1–22. https://doi.org/10.1007/BF01643440
Wiltschko, R. (2017). Navigation. Journal of Comparative Physiology A, 203(6), 455–463. https://doi.org/10.1007/s00359-017-1160-1
Wiltschko, R., Denzau, S., Gehring, D., Thalau, P. & Wiltschko, W. (2011). Magnetic orientation of migratory robins, Erithacus rubecula, under long-wavelength light. Journal of Experimental Biology, 214(18), 3096–3101. https://doi.org/10.1242/ jeb.059212
Wiltschko, R., Munro, U., Ford, H., Stapput, K., Thalau, P. & Wiltschko, W. (2014). Orientation of migratory birds under ultraviolet light. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 200(5), 399–407. https://doi.org/10.1007/s00359-014-0898-y
Wiltschko, R., Munro, U., Ford, H. & Wiltschko, W. (1999a). After-Effects of Exposure to Conflicting Celestial and Magnetic Cues at Sunset in Migratory Silvereyes Zosterops l. Lateralis. Journal of Avian Biology, 30(1), 56–62. https://doi.org/10.2307/3677243
Wiltschko, R., Munro, U., Ford, H. & Wiltschko, W. (2001a). Orientation in migratory birds: Time-associated relearning of celestial cues. Animal Behaviour, 62(2), 245–250. https://doi.org/10.1006/anbe.2001.1751
Wiltschko, R., Munro, U., Ford, H. & Wiltschko, W. (2008). Contradictory results on the role of polarized light in compass calibration in migratory songbirds. Journal of Ornithology, 149(4), 607–614. https://doi.org/10.1007/s10336-008-0324-8
Wiltschko, R., Siegmund, B. & Stapput, K. (2005). Navigational strategies of homing pigeons at familiar sites: Do landmarks reduce the deflections induced by clock-shifting? Behavioral Ecology and Sociobiology, 59(2), 303–312. https://doi.org/10.1007/s00265-005-0043-6
Wiltschko, R., Stapput, K., Thalau, P. & Wiltschko, W. (2010). Directional orientation of birds by the magnetic field under different light conditions. Journal of The Royal Society Interface, 7(suppl_2), S163–S177. https://doi.org/10.1098 /rsif.2009.0367.focus
Wiltschko, R. & Wiltschko, W. (1981a). The development of sun compass orientation in young homing pigeons. Behavioral Ecology and Sociobiology, 9(2), 135–141. https://doi.org/10.1007/BF00293584
Wiltschko, R. & Wiltschko, W. (1995a). Magnetic Orientation in Animals. Springer-Verlag. https://doi.org/10.100 7/978-3-642-79749-1
Wiltschko, R. & Wiltschko, W. (1998). Pigeon Homing: Effect of Various Wavelengths of Light During Displacement. Naturwissenschaften, 85(4), 164–167. https://doi.org/10.1007/s001140050476
Wiltschko, R. & Wiltschko, W. (2015). Avian Navigation: A Combination of Innate and Learned Mechanisms. Advances in the Study of Behavior, 47, 229–310. https://doi.org/10.1016/bs.asb.2014.12.002
Wiltschko, W. & Wiltschko, R. (1995b). Migratory orientation of European Robins is affected by the wavelength of light as well as by a magnetic pulse. Journal of Comparative Physiology A, 177(3), 363–369. https://doi.org/10.10 07/BF00192425
Wiltschko, W. & Wiltschko, R. (1999). The effect of yellow and blue light on magnetic compass orientation in European robins, Erithacus rubecula. Journal of Comparative Physiology A, 184(3), 295–299. https://doi.org/10.10 07/s003590050327
Wiltschko, W., Wiltschko, R., Munro, U. & Ford, H. (1998). Magnetic versus celestial cues: Cue-conflict experiments with migrating silvereyes at dusk. Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, 182(4), 521–529. https://doi.org/10.10 07/s003590050199
Wiltschko, W. (1968). Über den Einfluß statischer Magnetfelder auf die Zugorientierung der Rotkehlchen (Erithacus rubecula). Zeitschrift Für Tierpsychologie, 25(5), 537–558. https://doi.org/10.1111/j.1439-0310.1968.tb 00028.x
Wiltschko, W. (1978). Further Analysis of the Magnetic Compass of Migratory Birds. In Klaus Schmidt-Koenig & W. T. Keeton (Eds.), Animal Migration, Navigation, and Homing (pp. 302–310). Springer. https://doi.org/10.1007/978-3-662-11147-5_29
Wiltschko, W. (1983). Compasses used by birds. Comparative Biochemistry and Physiology Part A: Physiology, 76(4), 709–717. https://doi.org/10.1016/0300-9629(83)90132-9
Wiltschko, W., Balda, R. P., Jahnel, M. & Wiltschko, R. (1999b). Sun compass orientation in seed-caching corvids: Its role in spatial memory. Animal Cognition, 2(4), 215–221. https://doi.org/10.1007/s100710050042
Wiltschko, W., Daum, P., Fergenbauer-Kimmel, A. & Wiltschko, R. (1987). The development of the star compass in garden warblers, Sylvia borin. Ethology, 74(4), 285–292. https://doi.org/10.1111/j.1439-0310.1987.tb 00 939.x
Wiltschko, W., Freire, R., Munro, U., Ritz, T., Rogers, L., Thalau, P. & Wiltschko, R. (2007). The magnetic compass of domestic chickens, Gallus gallus. Journal of Experimental Biology, 210(13), 2300–2310. https://doi.org/10.1242/jeb.004853
Wiltschko, W., Gesson, M. & Wiltschko, R. (2001b). Magnetic compass orientation of European robins under 565 nm green light. Naturwissenschaften, 88(9), 387–390. https://doi.org/10.1007/s001140100248
Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. (1993). Red light disrupts magnetic orientation of migratory birds. Nature, 364(6437), 525–527. https://doi.org/10.1038/364525a0
Wiltschko, W. & Wiltschko, R. (1975a). The Interaction of Stars and Magnetic Field in the Orientation System of Night Migrating Birds. II. Spring experiments with European Robins (Erithacus rubecula). Zeitschrift Für Tierpsychologie, 39(1–5), 265–282. https://doi.org/10.1111/j.1439-0310.1975.tb00912.x
Wiltschko, W. & Wiltschko, R. (1975b). The interaction of stars and magnetic field in the orientation system of night migrating birds. I. Autumn experiments with European Warblers (gen. Sylvia). Zeitschrift Fur Tierpsychologie, 37(4), 337–355. https://doi.org/10.1 111/j.1439-0310.197 5.tb00885.x
Wiltschko, W. & Wiltschko, R. (1981b). Disorientation of inexperienced young pigeons after transportation in total darkness. Nature, 291(5814), 433–434. https://doi.org/1 0.1038/291433a0
Wiltschko, W., Wiltschko, R. & Keeton, W. T. (1976). Effects of a “permanent” clock-shift on the orientation of young homing pigeons. Behavioral Ecology and Sociobiology, 1(3), 229–243. https://doi.org/10.1007/BF00300066
Wu, L.-Q. & Dickman, J. D. (2011). Magnetoreception in an Avian Brain in Part Mediated by Inner Ear Lagena. Current Biology, 21(5), 418–423. https://doi.org/10.1016/j.cub.2011.01.058
Zapka, M., Heyers, D., Hein, C. M., Engels, S., Schneider, N.-L., Hans, J., Weiler, S., Dreyer, D., Kishkinev, D., Wild, J. M. & Mouritsen, H. (2009). Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature, 461(7268), 1274–1277. https://doi.org/10.1038/nature08528
Zhao, Y., Huang, Y.-N., Shi, L. & Chen, L. (2009). Analysis of magnetic elements in otoliths of the macula lagena in homing pigeons with inductively coupled plasma mass spectrometry. Neuroscience Bulletin, 25(3), 101–108. https://doi.org/10.1007/s12264-009-0311-y
Zink, G. & Bairlein, F. (1995). Der Zug europäischer Singvögel: Ein Atlas der Wiederfunde beringter Vögel (Vols. 1–5). Aula-Verlag.
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Orientation cues and mechanisms used during avian navigation: A review. (2021). Journal of Applied and Natural Science, 13(2), 627-640. https://doi.org/10.31018/jans.v13i2.2684