Abstract
Three compass systems based on global cues known to exist in migrating birds are reviewed. Two of these systems are based on celestial cues, a time-dependent sun compass and time-independent, i.e. not involving the internal clock, star compass. The third system is the magnetic compass, based on a separate sensory modality, which currently attracts much attention from behavioural ecologists, physiologists and physicists. The complex pattern of hierarchy and interactions between these compass systems is briefly discussed. It is argued that rules of integration of information from different compass cues are likely dependent on ecological and geographic conditions the birds are facing during their journey, so it is likely that no single set of rules is shared by all migrating birds.
Similar content being viewed by others
References
Åkesson S, Morin J, Muheim R, Ottosson U (2001) Avian orientation at steep angles of inclinations: experiments with migratory white-crowned sparrows at the magnetic North Pole. Proc R Soc Lond B 268:1907–1913
Åkesson S, Jonzen N, Pettersson J, Rundberg M, Sandberg R (2006) Effect of magnetic manipulations on orientation: comparing diurnal and nocturnal passerine migrants on Capri, Italy, in autumn. Ornis Svec 16:55–61
Åkesson S, Odin C, Hegedüs R, Ilieva M, Sjöholm C, Farkas A, Horváth G (2015) Testing avian compass calibration: comparative experiments with diurnal and nocturnal passerine migrants in south Sweden. Biol Open 4:35–47
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 10:0119919
Babushkina O, Bojarinova J (2011) Photoperiodically regulated cycle of locomotory activity and fat reserves during migration seasons in the irruptive bird species, the long-tailed tit (Aegithalos c. caudatus). J Avian Biol 42:169–177
Beason RC (1992) You can get there from here: responses to simulated magnetic equator crossing by the bobolink (Dolichonyx oryzivorus). Ethology 91:75–80
Bingman VP (1984) Night sky orientation of migratory pied flycatchers raised in different magnetic fields. Behav Ecol Sociobiol 15:77–80
Bingman VP (1987) Earth’s magnetism and the nocturnal orientation of migratory European robins. Auk 104:523–525
Bojarinova J, Babushkina O (2015) Photoperiodic conditions affect the level of locomotory activity during autumn migration in the Long-tailed Tit (Aegithalos c. caudatus). Auk 132:370–372
Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen L-O, van der Horst GTJ, Batschauer A, Ahmad M (2011) The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol 62:335–364
Chernetsov N (2015) Avian compass systems: do all migratory species possess all three? J Avian Biol 46:342–343
Chernetsov N, Kishkinev D, Kosarev V, Bolshakov CV (2011) Not all songbirds calibrate their magnetic compass from twilight cues: a telemetry study. J Exp Biol 214:2540–2543
Cochran WW, Mouritsen H, Wikelski M (2004) Migrating songbirds recalibrate their magnetic compass daily from twilight cues. Science 304:405–408
Duff SJ, Brownlie LA, Sherry DF, Sangster M (1998) Sun compass and landmark orientation by black-capped chickadees (Parus atricapillus). J Exp Biol 24:243–253
Emlen ST (1967a) Migratory orientation in the indigo bunting, Passerina cyanea. Part I: evidence of use of celestial cues. Auk 84:309–341
Emlen ST (1967b) Migratory orientation in the indigo bunting, Passerina cyanea. Part II: mechanism of celestial orientation. Auk 84:463–489
Emlen ST (1970) Celestial rotation: its importance in the development of migratory orientation. Science 170:1198–1201
Emlen ST (1975) The stellar-orientation system of a migratory bird. Sci Am 233:102–111
Emlen ST, Wiltschko W, Demong NJ, Wiltschko R, Bergman S (1976) Magnetic direction finding: evidence for its use in migratory indigo buntings. Science 193:505–508
Engels S, Schneider N-L, Lefeldt N, Hein CM, Zapka M, Michalik A, Elbers D, Kittel A, Hore PJ, Mouritsen H (2014) Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird. Nature 509:353–356
Finkelstein A, Las L, Ulanovsky N (2016) 3-D maps and compasses in the brain. Annu Rev Neurosci 39:171–196
Gill RE Jr, Tibbits TL, Douglas DC, Handel CM, Mulcahy DM, Gottschalck JC, Warnock N, McCaffery BJ, Battley PF, Piersma T (2009) Extreme endurance flights by landbirds crossing the Pacific Ocean: ecological corridor rather than barrier? Proc R Soc B 276:447–457
Heyers D, Manns M, Luksch H, Güntürkün O, Mouritsen H (2007) A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLoS ONE 2:e937
Hiscock SG, Worster S, Kattnig DR, Steers C, Jin Y, Manolopoulos ME, Mouritsen H, Hore PJ (2016) The quantum needle of the avian magnetic compass. Proc Natl Acad Sci USA 113:4634–4639
Hore PJ, Mouritsen H (2016) The radical-pair mechanism of magnetoreception. Annu Rev Biophys 45:299–344
Katz EB, Mihelson HA (1978) Impact of changing direction of stellar and magnetic meridian on European robin orientation in round cages in a planetarium. In: Mihelson HA (ed) Bird orientation. Zinatne, Riga, pp 180–193 (in Russian)
Kavokin K, Chernetsov N, Pakhomov A, Bojarinova J, Kobylkov D, Namozov B (2014) Magnetic orientation of garden warblers (Sylvia borin) under 1.4 MHz radiofrequency magnetic field. J R Soc Interface 11:20140451
Keeton W (1979) Avian orientation and navigation. Annu Rev Physiol 41:353–366
Kramer G (1950) Weitere Analyse der Faktoren, welche die Zugaktivität des gekäfigten Vogels orientieren. Naturwissenschaften 37:377–378
Kramer G, von Saint Paul U (1950) Stare lassen sich auf Himmelsrichtungen dressieren. Naturwissenschaften 37:526–527
Lefeldt N, Dreyer D, Schneider N-L, Steeken F, Mouritsen H (2015) Migratory blackcaps tested in Emlen funnels can orient at 85 degrees but not at 88 degrees magnetic inclination. J Exp Biol 218:206–211
Liu X, Chernetsov N (2012) Avian orientation: multi-cue integration and calibration of compass systems. Chin Birds 3:1–8
Merkel FW, Wiltschko W (1965) Magnetismus und Richtungsfinden zugunruhiger Rotkehlchen (Erithacus rubecula). Vogelwarte 23:71–77
Michalik A, Alert B, Engels S, Lefeldt N, Mouritsen H (2014) Star compass learning: How long does it take? J Ornithol 155:225–234
Moore FR (1985) Integration of environmental stimuli in the migratory orientation of the Savannah sparrow, Passerculus sandwichensis. Anim Behav 33:654–663
Mouritsen H (2015) Magnetoreception in birds and its use for long-distance migration. In: Scanes SG (ed) Sturkie’s avian physiology, 6th edn. Academic, London, pp 113–133
Mouritsen H, Larsen ON (2001) Migrating songbirds tested in computer-controlled Emlen funnels use stellar cues for a time-independent compass. J Exp Biol 204:3855–3865
Mouritsen H, Feenders G, Liedvogel M, Wada K, Jarvis ED (2005) Night-vision brain area in migratory songbirds. Proc Natl Acad Sci USA 102:8339–8344
Mouritsen H, Heyers D, Güntürkün O (2016) The neural basis of long-distance navigation in birds. Annu Rev Physiol 78:133–154
Muheim R, Moore FR, Phillips JB (2006a) Calibration of magnetic and celestial compass cues in migratory birds—a review of cue-conflict experiments. J Exp Biol 209:2–17
Muheim R, Phillips JB, Åkesson S (2006b) Polarized light cues underlie compass calibration in migratory songbirds. Science 313:837–839
Muheim R, Phillips JB, Deutschlander ME (2009) White-throated sparrows calibrate their magnetic compass by polarized light cues during both autumn and spring migration. J Exp Biol 212:3466–3472
Muheim R, Henshaw I, Sjöberg S, Deutschlander ME (2014) BirdOriTrack: a new video-tracking program for orientation research with migratory birds. J Field Ornithol 85:91–105
Munro U, Wiltschko R (1993a) Clock-shift experiments with migratory yellow-faced honeyeaters, Lichenostomus chrysops (Meliphagidae), an Australian day migrating bird. J Exp Biol 181:233–244
Munro U, Wiltschko R (1993b) Magnetic compass orientation in the yellow-faced honeyeater, Lichenostomus chrysops, a day migrating bird from Australia. Behav Ecol Sociobiol 32:141–145
Qin S, Yin H, Yang C, Dou Y, Liu Z, Zhang P, Yu H, Nuang 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 (2015) A magnetic protein biocompass. Nat Mater 15:217–226
Ritz T, Adem S, Schulten K (2000) A model for photoreceptor-based magnetoreception in birds. Biophys J 78:707–718
Ritz T, Thalau P, Phillips JB, Wiltschko R, Wiltschko W (2004) Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429:177–180
Sandberg R, Ottosson U, Pettersson J (1991) Magnetic orientation of migratory wheatears (Oenanthe oenanthe) in Sweden and Greenland. J Exp Biol 155:51–64
Sandberg R, Bäckman J, Moore FR, Lõhmus M (2000) Magnetic information calibrates celestial cues during migration. Anim Behav 60:453–462
Sauer F (1956) Zugorientierung einer Mönchsgrasmücke (Sylvia a. atricapilla, L.) unter künstlichem Sternenhimmel. Naturwissenschaften 43:231–232
Schmaljohann H, Rautenberg T, Muheim R, Naef-Daenzer B, Bairlein F (2013) Response of a free-flying songbird to an experimental shift of the light polarization pattern around sunset. J Exp Biol 216:1381–1387
Schmidt-Koenig K (1958) Experimentelle Einflußname aud die 24-Stunden-Periodik bei Brieftauben und deren Auswirkungen unter besonderer Berücksichtigung des Heimfindevermögens. Z Tierpsychol 15:301–331
Schulten K, Swenberg CE, Weller A (1978) A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion. Z Phys Chem (NF) 111:1–5
Schwarze S, Schneider N-L, Reichl T, Dreyer D, Lefeldt N, Engels S, Baker N, Hore PJ, Mouritsen H (2016a) Weak broadband electromagnetic field are more disruptive to magnetic compass orientation in a night-migratory songbird (Erithacus rubecula) than strong narrow-band fields. Front Behav Neurosci 10:55
Schwarze S, Steenken F, Thiele N, Kobylkov D, Lefeldt N, Dreyer D, Schneider N-L, Mouritsen H (2016b) Migratory blackcaps can use their magnetic compass at 5 degrees inclination, but are completely random at 0 degrees inclination. Sci Rep 6:33805
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 conflict experiments with migratory songbirds. Front Behav Neurosci 10:29
Solov’yov IA, Schulten K (2009) Magnetoreception through cryptochrome may involve superoxide. Biophys J 96:4804–4813
Thalau P, Ritz T, Stapput K, Wiltschko R, Wiltschko W (2005) Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften 92:86–90
von Middendorff AT (1855) Die Isopiptesen Russlands. Grundlagen zur Erforschung der Zugzeiten und Zugrichtungen der Vögel Russlands. Mem Acad Sci St Petersbg Sci Nat 8:1–143
Voss J, Keary N, Bischof H-J (2007) The use of the geomagnetic field for short-distance orientation in zebra finches. Behaviour 18:1053–1057
Weindler P, Beck W, Liepa V, Wiltschko W (1995) Development of migratory orientation in pied flycatchers in different magnetic inclinations. Anim Behav 49:227–234
Wiltschko W (1968) Über den Einfluß statischer Magnetfelder auf die Zugorientierung der Rotkehlchen (Erithacus rubecula). Z Tierpsychol 25:537–558
Wiltschko W (1974) Der Magnetkompass der Gartengrasmücke (Sylvia borin). J Ornithol 115:1–7
Wiltschko W (1978) Further analysis of the magnetic compass of migratory birds. In: Schmidt-Koenig K, Keeton WT (eds) Animal migration, navigation, and homing. Springer, Berlin, pp 302–310
Wiltschko R (2017) Navigation. J Comp Physiol A (this volume)
Wiltschko W, Balda RP (1989) Sun compass orientation in seed-caching scrub jays (Aphelocoma coerulescens). J Comp Physiol A 164:717–721
Wiltschko R, Nehmzow U (2005) Simulating pigeon navigation. Anim Behav 69:813–826
Wiltschko W, Wiltschko R (1972) Magnetic compass of European robins. Science 176:62–64
Wiltschko R, Wiltschko W (1980) The process of learning sun compass orientation in young homing pigeons. Naturwissenschaften 67:512–514
Wiltschko R, Wiltschko W (1990a) The development of sun compass orientation in young homing pigeons. J Ornithol 131:1–19
Wiltschko W, Wiltschko R (1990b) Magnetic orientation and celestial cues in migratory orientation. Experientia 46:342–352
Wiltschko W, Wiltschko R (1992) Migratory orientation: magnetic compass orientation of garden warblers (Sylvia borin) after a simulated crossing of the magnetic equator. Ethology 91:70–74
Wiltschko R, Wiltschko W (1999) Celestial and magnetic cues in experimental conflict. In: Adams NJ, Slotow RH (eds) Proceedings of the 22nd international ornithology congress Durban. BirdLife South Africa, Johannesburg, pp 988–1004
Wiltschko W, Wiltschko R (2001) Light-dependent magnetoreception in birds: the behaviour of European robins, Erithacus rubecula, under monochromatic light of various wavelengths and intensities. J Exp Biol 204:3295–3302
Wiltschko R, Wiltschko W (2015) Avian navigation: a combination of innate and learned mechanisms. Adv Study Behav 47:229–310
Wiltschko W, Wiltschko R, Keeton WT (1976) Effects of a “permanent” clock-shift on the orientation of young homing pigeons. Behav Ecol Sociobiol 1:229–243
Wiltschko W, Wiltschko R, Keeton WT (1984) The effect of a “permanent” clockshift on the orientation of experienced homing pigeons. I. Experiments in Ithaca, New York, USA. Behav Ecol Sociobiol 15:263–272
Wiltschko W, Daum P, Fergenbauer-Kimmel A, Wiltschko R (1987) The development of the star compass in garden warblers, Sylvia borin. Ethology 74:285–292
Wiltschko W, Munro U, Ford H, Wiltschko R (1993) Red light disrupts magnetic orientation of migratory birds. Nature 364:525–527
Wiltschko W, Weindler P, Wiltschko R (1998) Interaction of magnetic and celestial cues in the migratory orientation of passerines. J Avian Biol 29:606–617
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 lateralis. J Avian Biol 30:56–62
Wiltschko W, Balda RP, Jahnel M, Wiltschko R (1999b) Sun compass orientation in seed-caching corvids: its role in spatial memory. Anim Cogn 2:215–221
Wiltschko W, Wiltschko R, Munro U (2000) Light-dependent magnetoreception in birds: the effect of intensity of 565 nm green light. Naturwissenschaften 87:366–369
Wiltschko R, Munro U, Ford H, Wiltschko W (2001a) Orientation in migratory birds: time-associated relearning of celestial cues. Anim Behav 62:245–250
Wiltschko W, Gesson M, Wiltschko R (2001b) Magnetic compass orientation of European robins under 565 nm green light. Naturwissenschaften 88:387–390
Wiltschko W, Freire R, Munro U, Ritz T, Rogers L, Thalau P, Wiltschko R (2007) The magnetic compass of domestic chickens, Gallus gallus. J Exp Biol 210:2300–2310
Wiltschko R, Munro U, Ford H, Wiltschko W (2008) Contradictory results on the role of polarized light in compass calibration in migratory songbirds. J Ornithol 149:607–614
Zapka M, Heyers D, Hein CM, Engels S, Schneider N-L, Hans J, Weiler S, Dreyer D, Kishkinev D, Wild JM, Mouritsen H (2009) Visual, but not trigeminal, mediation of magnetic compass information in a migratory bird. Nature 461:1274–1277
Zapka M, Heyers D, Liedvogel M, Jarvis ED, Mouritsen H (2010) Night-time neuronal activation of Cluster N in a day- and night-migrating songbird. Eur J Neurosci 32:619–624
Acknowledgements
This study has been supported by a grant 16-14-10159 from the Russian Science Foundation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that he has no conflict of interests.
Rights and permissions
About this article
Cite this article
Chernetsov, N. Compass systems. J Comp Physiol A 203, 447–453 (2017). https://doi.org/10.1007/s00359-016-1140-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-016-1140-x