Journal of Ornithology

, Volume 156, Supplement 1, pp 145–161

Sensory mechanisms of long-distance navigation in birds: a recent advance in the context of previous studies

Review

Abstract

Displacement studies have clearly shown that experienced avian migrants are able to perform true navigation, i.e., they can find the correct direction leading to a target destination from unfamiliar sites. The sensory mechanisms of true navigation remain poorly understood, though some remarkable progress has been made in the last 10–15 years. There are two primary hypotheses explaining the sensory nature of navigation: (1) a magnetic map hypothesis proposes that birds use parameters of the geomagnetic field that are predictably distributed on the globe. As for the sensory nature of this hypothesis, it has been assumed by some researchers that the magnetic receptor cells reside in the upper beak (the so-called “beak organ”), and transmit information via the trigeminal nerve to the brain; (2) an olfactory map hypothesis assumes that birds can smell their position by taking advantage of odours distributed in the atmosphere. There are a growing number of studies supporting both of the hypotheses mentioned though in different avian model species. In this review, an attempt is made to provide an overview of the evidence for different navigational cues proposed thus far, with the main focus on the recent studies addressing the magnetic and olfactory navigation hypotheses. Also, a list of key open questions, together with possible experimental approaches, is proposed.

Keywords

True navigation Navigational cues Olfactory navigation Magnetic navigation Trigeminal system 

References

  1. Able KP, Cherry JD (1986) Mechanisms of dusk orientation in white-throated sparrows (Zonotrichia albicollis): clock-shift experiments. J Comp Physiol A 159:107–113CrossRefGoogle Scholar
  2. Able KP, Dillon PM (1977) Sun compass orientation in a nocturnal migrant white-throated sparrow. Condor 79:393–395CrossRefGoogle Scholar
  3. Åkesson S (1993) Coastal migration and wind drift compensation in nocturnal passerine migrants. Ornis Scand 24:87–94CrossRefGoogle Scholar
  4. Alerstam T, Hake M, Kjellen N (2006) Temporal and spatial patterns of repeated migratory journeys by ospreys. Anim Behav 71:555–566CrossRefGoogle Scholar
  5. Batschelet E (1981) Circular statistics in biology. Academic Press, LondonGoogle Scholar
  6. Beason R, Semm P (1996) Does the avian ophthalmic nerve carry magnetic navigational information? J Exp Biol 199:1241–1244PubMedGoogle Scholar
  7. Becker J, van Raden H (1986) Meteorologische Gesichtspunkte zur olfaktorischen Navigationshypothese. J Ornithol 127:1–8CrossRefGoogle Scholar
  8. Benhamou S (1997) On systems of reference involved in spatial memory. Behav Process 40:149–163CrossRefGoogle Scholar
  9. Benhamou S (2003) Bicoordinate navigation based on non-orthogonal gradient fields. J Theor Biol 225:235–239PubMedCrossRefGoogle Scholar
  10. Benhamou S, Bovet P (1989) How animals use their environment: a new look at kinesis. Anim Behav 38:375–383CrossRefGoogle Scholar
  11. Benhamou S, Bonadonna F, Jouventin P (2003) Successful homing of magnet-carrying white-chinned petrels released in the open sea. Anim Behav 65:729–734CrossRefGoogle Scholar
  12. Benvenuti S, Brown IA (1989) The influence of olfactory deprivation on homing of experienced and inexperienced American pigeons. Behaviour 111:113–128CrossRefGoogle Scholar
  13. Berthold P (1988) Evolutionary aspects of migratory behavior in European warblers. J Evol Biol 1:195–209CrossRefGoogle Scholar
  14. Berthold P, Querner U (1981) Genetic basis of migratory behavior in European warblers. Science 212:77–79PubMedCrossRefGoogle Scholar
  15. Berthold P, Wiltschko W, Miltenberger H, Querner U (1990) Genetic transmission of migratory behavior into a non-migratory bird population. Experientia 46:107–108CrossRefGoogle Scholar
  16. Blaser N, Guskov SI, Meskenaite V, Kanevskyi VA, Lipp H-P (2013) Altered orientation and flight paths of pigeons reared on gravity anomalies: a GPS tracking study. PLoS One 8:e77102PubMedPubMedCentralCrossRefGoogle Scholar
  17. Blaser N, Guskov SI, Entin VA, Wolfer DP, Kanevskyi VA, Lipp H-P (2014) Gravity anomalies without geomagnetic disturbances interfere with pigeon homing – a GPS tracking study. J Exp Biol 217:4057–4067PubMedCrossRefGoogle Scholar
  18. Bonadonna F, Chamaille-Jammes S, Pinaud D, Weimerskirch H (2003) Magnetic cues: are they important in black-browed albatross Diomedea malanophris orientation? Ibis 145:152–155CrossRefGoogle Scholar
  19. Boström JE, Åkesson S, Alerstam T (2012) Where on earth can animals use a geomagnetic bi-coordinate map for navigation? Ecography 35:1039–1047CrossRefGoogle Scholar
  20. Bubień-Waluszewska A (1981) The cranial nerves. In: King AS, McLelland J (eds) Form and function in birds, vol 2. Academic Press, New York, pp 385–438Google Scholar
  21. Cadiou H, McNaughton PA (2010) Avian magnetite-based magnetoreception: a physiologist’s perspective. J R Soc Interface 7:S193–S205PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chernetsov N, Kishkinev D, Mouritsen H (2008) A long-distance avian migrant compensates for longitudinal displacement during spring migration. Curr Biol 18:188–190PubMedCrossRefGoogle Scholar
  23. Cygnar KD, Stephan AB, Zhao H (2010) Analyzing responses of mouse olfactory sensory neurons using the air-phase electroolfactogram recording. J Vis Exp 37:e1850Google Scholar
  24. de la Iglesia HO, Cambras T, Schwartz WJ, Díez-Noguera A (2004) Forced desynchronization of dual circadian oscillators within the rat suprachiasmatic nucleus. Curr Biol 14:796–800PubMedCrossRefGoogle Scholar
  25. Delahunty CM, Eyres G, Dufour J-P (2006) Gas chromatography-olfactometry. J Sep Sci 29:2107–2125PubMedCrossRefGoogle Scholar
  26. Delmore KE, Irwin DE (2014) Hybrid songbirds employ intermediate routes in a migratory divide. Ecol Lett 17:1211–1218PubMedCrossRefGoogle Scholar
  27. Deutschlander ME, Phillips JB, Munro U (2012) Age-dependent orientation to magnetically-simulated geographic displacements in migratory Australian silvereyes (Zosterops l. lateralis). Wils J Ornithol 124:467–477CrossRefGoogle Scholar
  28. Dornfeldt K (1991) Pigeon homing in relation to geomagnetic, gravitational, topographical, and meteorological conditions. Behav Ecol Sociobiol 28:107–123CrossRefGoogle Scholar
  29. Dubbeldam JL, Brauch CSM, Don A (1981) Studies on the somatotopy of the trigeminal system in the mallard, Anas platyrhynos L.: the afferents and organisation of the nucleus basalis. J Comp Neurol 196:391–405PubMedCrossRefGoogle Scholar
  30. Edelman NB, Fritz T, Nimpf S, Pichler P, Lauwers M et al (2014) No evidence for intracellular magnetite in putative vertebrate magnetoreceptors identified by magnetic screening. Proc Natl Acad Sci 112:262–267PubMedPubMedCentralCrossRefGoogle Scholar
  31. Emlen ST (1967a) Migratory orientation in the indigo bunting, Passerina cyanea. Part I: evidence for use of celestial cues. Auk 84:309–342CrossRefGoogle Scholar
  32. Emlen ST (1967b) Migratory orientation in the indigo bunting, Passerina cyanea. Part II: mechanism of celestial orientation. Auk 84:463–489CrossRefGoogle Scholar
  33. Emlen ST (1975) The stellar-orientation system of a migratory bird. Sci Am 233:102–111PubMedCrossRefGoogle Scholar
  34. Falkenberg G, Fleissner G, Schuchardt K, Kuehbacher M, Thalau P et al (2010) Avian magnetoreception: elaborate iron mineral containing dendrites in the upper beak seem to be a common feature of birds. PLoS One 5:e9231PubMedPubMedCentralCrossRefGoogle Scholar
  35. Fiaschi V, Farina M, Ioalè P (1974) Homing experiments on swifts Apus apus (L.) deprived of olfactory perception. Monit Zool Ital 8:235–244Google Scholar
  36. Fischer RG, Kastler J, Ballschmiter K (2000) Levels and pattern of alkyl nitrates, multifunctional alkyl nitrates, and halocarbons in the air over the Atlantic Ocean. J Geophys Res 10:14473–14494CrossRefGoogle Scholar
  37. Fischer JH, Munro U, Phillips JB (2003) Magnetic navigation by an avian migrant? In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer Verlag, Berlin, Heidelberg, pp 423–432CrossRefGoogle Scholar
  38. Fleissner G, Holtkamp-Rötzler E, Hanzlik M, Winklhofer M, Fleissner G et al (2003) Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J Comp Neurol 458:350–360PubMedCrossRefGoogle Scholar
  39. Fleissner G, Stahl B, Thalau P, Falkenberg G, Fleissner G (2007) A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons. Naturwiss 94:631–642PubMedCrossRefGoogle Scholar
  40. Gagliardo A (2013) Forty years of olfactory navigation in birds. J Exp Biol 216:2165–2171PubMedCrossRefGoogle Scholar
  41. Gagliardo A, Odetti F, Ioalè P (2001) Relevance of visual cues for orientation at familiar sites by homing pigeons: an experiment in a circular arena. Proc R Soc B 268:2065–2070PubMedPubMedCentralCrossRefGoogle Scholar
  42. Gagliardo A, Ioalè P, Savini M, Wild JM (2006) Having the nerve to home: trigeminal magnetoreceptor versus olfactory mediation of homing in pigeons. J Exp Biol 209:2888–2892PubMedCrossRefGoogle Scholar
  43. Gagliardo A, Ioalè P, Savini M, Wild JM (2008) Navigational abilities of homing pigeons deprived of olfactory or trigeminally mediated magnetic information when young. J Exp Biol 211:2046–2051PubMedCrossRefGoogle Scholar
  44. Gagliardo A, Ioalè P, Savini M, Wild JM (2009) Navigational abilities of adult and experienced homing pigeons deprived of olfactory or trigeminally mediated magnetic information. J Exp Biol 212:3119–3124PubMedCrossRefGoogle Scholar
  45. Gagliardo A, Ioalè P, Filaninno 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:e22385PubMedPubMedCentralCrossRefGoogle Scholar
  46. 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. J Exp Biol 216:2798–2805PubMedCrossRefGoogle Scholar
  47. Gottschaldt K-M (1985) Structure and function of avian somatosensory receptors. In: King AS, McLelland J (eds) Form and function in birds, vol 3. Academic Press, New York, pp 375–461Google Scholar
  48. Gould JL (1980) The case of magnetic sensitivity in birds and bees (such as it is). Am Sci 68:256–267Google Scholar
  49. Griffin DR (1952) Bird navigation. Biol Rev Cambr Philos Soc Lond 27:359–400CrossRefGoogle Scholar
  50. Gschweng M, Kalko EKV, Querner U, Fiedler W, Berthold P (2008) All across Africa: highly individual migration routes of Eleonora’s falcon. Proc R Soc B 275:2887–2896PubMedPubMedCentralCrossRefGoogle Scholar
  51. Guilford T, Biro D (2014) Route following and the pigeon’s familiar area map. J Exp Biol 217:169–179PubMedCrossRefGoogle Scholar
  52. Guilford T, Taylor GK (2014) The sun compass revisited. Anim Behav 97:135–143PubMedPubMedCentralCrossRefGoogle Scholar
  53. Gwinner E (1996a) Circadian and circannual programmes in avian migration. J Exp Biol 199:39–48PubMedGoogle Scholar
  54. Gwinner E (1996b) Circannual clocks in avian reproduction and migration. Ibis 138:47–63CrossRefGoogle Scholar
  55. Gwinner E (2003) Circannual rhythms in birds. Curr Opin Neurobiol 13:770–778PubMedCrossRefGoogle Scholar
  56. Hagstrum JT (2000) Infrasound and the avian navigational map. J Exp Biol 203:1103–1111PubMedGoogle Scholar
  57. Hagstrum JT (2001) Infrasound and the avian navigational map. J Nav 54:377–391Google Scholar
  58. Hagstrum JT (2013) Atmospheric propagation modeling indicates homing pigeons use loft-specific infrasonic’map’ cues. J Exp Biol 216:687–699PubMedCrossRefGoogle Scholar
  59. Hanzlik M, Heunemann C, Holtkamp-Rötzler E, Winklhofer M, Petersen N, Fleissner G (2000) Superparamagnetic magnetite in the upper beak tissue of homing pigeons. Biometals 13:325–331PubMedCrossRefGoogle Scholar
  60. Helbig AJ (1991) Inheritance of migratory direction in a bird species: a cross-breeding experiment with SE- and SW-migrating blackcaps (Sylvia atricapilla). Behav Ecol Sociobiol 28:9–12CrossRefGoogle Scholar
  61. Heyers D, Zapka M, Hoffmeister M, Wild JM, Mouritsen H (2010) Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. Proc Natl Acad Sci USA 107:9394–9399PubMedPubMedCentralCrossRefGoogle Scholar
  62. Hirt C, Claessens S, Fecher T, Kuhn M, Pail R, Rexer M (2013) New ultrahigh-resolution picture of earth’s gravity field. Geophys Res Lett 40:4279–4283CrossRefGoogle Scholar
  63. Holland RA (2010) Differential effects of magnetic pulses on the departure directions of naturally migrating birds. J R Soc Interface 7:1617–1625PubMedPubMedCentralCrossRefGoogle Scholar
  64. Holland RA, Thorup K, Gagliardo A, Bisson IA, Knecht E et al (2009) Testing the role of sensory systems in the migratory heading of a songbird. J Exp Biol 212:4065–4071PubMedCrossRefGoogle Scholar
  65. Ioalè P (1983) Effect of anaesthesia of the nasal mucosae on the homing behaviour of pigeons. Z Tierpsychol 61:102–110Google Scholar
  66. Ioalè P, Wallraff HG, Papi F, Foà A (1983) Long-distance releases to determine the spatial range of pigeon navigation. Comp Biochem Physiol 76A:733–742CrossRefGoogle Scholar
  67. Ioalè P, Nozzolini M, Papi F (1990) Homing pigeons do extract directional information from olfactory stimuli. Behav Ecol Sociobiol 26:301–305CrossRefGoogle Scholar
  68. Jorge PE, Marques AE, Phillips JB (2009) Activational rather than navigational effects of odours on homing of young pigeons. Curr Biol 19:650–654PubMedCrossRefGoogle Scholar
  69. Jorge PE, Marques AE, Phillips (2010) Activational effects of odours on avian navigation. Proc R Soc B 277:45–49PubMedPubMedCentralCrossRefGoogle Scholar
  70. Kanevskyi VA, Sitnik KM, Sheliag-Sosonko JP, Melnikov DI, Dima AG et al (1985) The use of biotelemetry in remote sensing of geophysical parameters. Rep Acad Sci USSR 282:291–294Google Scholar
  71. Kishkinev D, Chernetsov N (2015) Magnetoreception systems in birds. Biol Bull Rev 5:46–62. doi:10.1134/S2079086415010041 CrossRefGoogle Scholar
  72. Kishkinev D, Chernetsov N, Mouritsen H (2010) A double clock or jetlag mechanism is unlikely to be involved in detection of east-west displacements in a long-distance avian migrant. Auk 127:773–780CrossRefGoogle Scholar
  73. Kishkinev D, Mora CV, Mouritsen H (2012) An attempt to develop an operant conditioning paradigm to test for magnetic discrimination behaviour in a migratory songbird. J Ornithol 153:1165–1177CrossRefGoogle Scholar
  74. Kishkinev D, Chernetsov N, Heyers D, Mouritsen H (2013) Migratory reed warblers need intact trigeminal nerve to correct for a 1,000 km eastward displacement. PLoS ONE 8:e65847PubMedPubMedCentralCrossRefGoogle Scholar
  75. Kramer G (1950a) Orientierte Zugaktivität gekäfigter Singvögel. Naturwiss 37:188CrossRefGoogle Scholar
  76. Kramer G (1950b) Weitere analyse der Faktoren, welche die Zugaktivität des gekäfigten Vögels orientieren. Naturwiss 37:377–378CrossRefGoogle Scholar
  77. Kramer G (1953) Wird die Sonnehöhe bei der Heimfindeorientierung verwertet? J Ornithol 94:201–219CrossRefGoogle Scholar
  78. Kullberg C, Lind J, Fransson T, Jakobsson S, Vallin A (2003) Magnetic cues and time of season affect fuel deposition in migratory thrush nightingales (Luscinia luscinia). Proc R Soc B 270:373–378PubMedPubMedCentralCrossRefGoogle Scholar
  79. Kullberg C, Henshaw I, Jakobsson S, Johansson P, Fransson T (2007) Fuelling decisions in migratory birds: geomagnetic cues override the seasonal effect. Proc R Soc B 274:2145–2151PubMedPubMedCentralCrossRefGoogle Scholar
  80. Larkin T, Keeton WT (1978) An apparent lunar rhythm in the day-to-day variations in initial bearings of homing pigeons. In: Schmidt-Koenig K, Keeton WT (eds) Animal migration, navigation and homing. Springer-Verlag, Berlin, New York, pp 92–106CrossRefGoogle Scholar
  81. Lauwers M, Pichler P, Edelman NB, Resch GP, Ushakova L et al (2013) An iron-rich organelle in the cuticular plate of avian hair cells. Curr Biol 23:924–929PubMedCrossRefGoogle Scholar
  82. Lednor AJ, Walcott C (1984) The orientation of pigeons at gravity anomalies. J Exp Biol 111:259–263Google Scholar
  83. Lefeldt N, Heyers D, Schneider NL, Engels S, Elbers D, Mouritsen H (2014) Magnetic field-driven induction of ZENK in the trigeminal system of pigeons (Columba livia). J R Soc Interface 11:20140777PubMedPubMedCentralCrossRefGoogle Scholar
  84. Liedvogel M, Akesson S, Bensch S (2011) The genetics of migration on the move. Trends Ecol Evol 26:561–569PubMedCrossRefGoogle Scholar
  85. Massa B, Benvenuti S, Ioalè P, Lo Valvo M, Papi F (1991) Homing in Cory’s shearwater (Calonectris diomedea) carrying magnets. Boll Zoll 58:245–247CrossRefGoogle Scholar
  86. Matthews GVT (1951) The experimental investigation of navigation in homing pigeons. J Exp Biol 28:508–536Google Scholar
  87. Matthews GVT (1953) Sun navigation in homing pigeons. J Exp Biol 30:243–267Google Scholar
  88. Mebius RE, Kraal G (2005) Structure and function of the spleen. Nature Rev Immunol 5:606–616CrossRefGoogle Scholar
  89. Meschini E (1983) Pigeon navigation: some experiments on the importance of olfactory cues at short distances from the loft. J Comp Physiol 150:493–498CrossRefGoogle Scholar
  90. Mewaldt R (1964) California sparrows return from displacement to Maryland. Science 146:941–942PubMedCrossRefGoogle Scholar
  91. Moore BR (1988) Magnetic fields and orientation in homing pigeons: experiments of the late W.T Keeton. Proc Natl Acad Sci USA 85:4907–4909PubMedPubMedCentralCrossRefGoogle Scholar
  92. Mora CV, Walker MM (2012) Consistent effect of an attached magnet on the initial orientation of homing pigeons, Columba livia. Anim Behav 84:377–383CrossRefGoogle Scholar
  93. Mora CV, Davison M, Wild JM, Walker MM (2004) Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432:508–511PubMedCrossRefGoogle Scholar
  94. Mouritsen H (2003) Spatiotemporal orientation strategies of long-distance migrants. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian Migration. Springer Verlag, Berlin, Heidelberg, pp 493–513CrossRefGoogle Scholar
  95. Mouritsen H, Hore PJ (2012) The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds. Curr Opin Neurobiol 22:343–352PubMedCrossRefGoogle Scholar
  96. Mouritsen H, Larsen ON (2001) Migrating songbirds tested in computer-controlled Emlen funnels use stellar cues for a time-independent compass. J Exp Biol 204:3855–3865PubMedGoogle Scholar
  97. Mouritsen H, Huyvaert KP, Frost BJ, Anderson DJ (2003) Waved albatrosses can navigate with strong magnets attached to their head. J Exp Biol 206:4155–4166PubMedCrossRefGoogle Scholar
  98. Muheim R, Åkesson S (2002) Clock-shift experiments with Savannah sparrows, Passerculus sandwichensis, at high northern latitudes. Behav Ecol Sociobiol 51:394–401CrossRefGoogle Scholar
  99. Nevitt G (2008) Sensory ecology on the high seas: the odour world of the Procellariiform seabirds. J Exp Biol 211:1706–1713PubMedCrossRefGoogle Scholar
  100. Newton I (2008) The migration biology of birds. Academic Press, LondonGoogle Scholar
  101. Papi F (1975) La navigazione dei colombi viaggiatori. Le Scienze 78:66–75Google Scholar
  102. Papi F (1976) The olfactory navigation system of homing pigeons. Verh Dtsch Zool Ges 69:184–205Google Scholar
  103. Papi F, Fiore L, Fiaschi V, Benvenuti S (1972) Olfaction and homing in pigeons. Monit Zool Ital 6:85–95Google Scholar
  104. Papi F, Ioalè P, Fiaschi V, Benvenuti S, Baldaccini NE (1974) Olfactory navigation of pigeons: the effect of treatment with odourous air currents. J Comp Physiol 94:187–193CrossRefGoogle Scholar
  105. Pennycuick CJ (1960) The physical basis of astronavigation in birds: theoretical considerations. J Exp Biol 37:573–593Google Scholar
  106. Pennycuick CJ (1961) Sun navigation in birds? Nature 190:1127–1128CrossRefGoogle Scholar
  107. Perdeck AC (1958) Two types of orientation in migrating starlings, Sturnus vulgaris L., and chaffinches, Fringilla coelebs L., as revealed by displacement experiments. Ardea 46:1–37Google Scholar
  108. Perdeck A (1983) An experiment on the orientation of juvenile starlings during spring migration: an addendum. Ardea 71:255Google Scholar
  109. Phillip JB (1996) Magnetic navigation. J Theor Biol 180:309–319CrossRefGoogle Scholar
  110. Piggins HD, Loudon (2005) Circadian biology: clocks within clocks. Curr Biol 15:R455–R457PubMedCrossRefGoogle Scholar
  111. Postlethwaite CM, Walker MM (2011) A geometric model for initial orientation errors in pigeon navigation. J Theor Biol 269:273–279PubMedCrossRefGoogle Scholar
  112. Rabøl J (1998) Star navigation in Pied Flycatchers Ficedula hypoleuca and redstarts Phoenicurus phoenicurus. Dansk Ornitologisk Forenings Tidsskrift 92:283–289Google Scholar
  113. Rehkämper G, Frahm H, Cnotka J (2008) Mosaic evolution and adaptive brain component alteration under domestication seen on the background of evolutionary theory. Brain Behav Evol 71:115–126PubMedCrossRefGoogle Scholar
  114. Reilly IW (2002) Magnetic position determination by homing pigeons? J Theor Biol 218:47–54CrossRefGoogle Scholar
  115. Renfrew RB, Kim D, Perlut N, Smith J, Fox J, Marra PP (2013) Phenological matching across hemispheres in a long-distance migratory bird. Divers Distrib 19:1008–1019CrossRefGoogle Scholar
  116. Sauer F (1957) Die Sternenorientierung nächtlich ziehender Grasmücken (Sylvia atricapilla, borin and curruca). Z Tierpsychol 14:29–70Google Scholar
  117. Sauer FEG, Sauer EM (1960) Star navigation of nocturnal migrating birds: the 1958 planetarium experiments. Cold Spring Harb Symp Quant Biol 25:463–473PubMedCrossRefGoogle Scholar
  118. Schmidt-Koenig K (1960) The sun azimuth compass: one factor in the orientation of homing pigeons. Science 131:826–827PubMedCrossRefGoogle Scholar
  119. Schmidt-Koenig K, Ganzhorn JU, Ranvaud R (1991) The sun compass. Experientia Supplementum 60:1–15CrossRefGoogle Scholar
  120. Smith AD, Paton PW, McWilliams SR (2014) Using nocturnal flight calls to assess the fall migration of warblers and sparrows along a coastal ecological barrier. PLoS One 9:e92218PubMedPubMedCentralCrossRefGoogle Scholar
  121. Sokolov L (1997) Philopatry of migratory birds. In: Turpaev TM (ed) Physiology and general biology reviews,v. 11. Harwood Academic Press, Amsterdam, pp 1–58Google Scholar
  122. Stanley CQ, MacPherson M, Fraser KC, McKinnon EA, Stutchbury BJM (2012) Repeat tracking of individual songbirds reveals consistent migration timing but flexibility in route. PLoS One 7:e40688PubMedPubMedCentralCrossRefGoogle Scholar
  123. Streng A, Wallraff HG (1992) Attempts to determine the roles of visual and olfactory inputs in initial orientation and homing of pigeons over familiar terrain. Ethology 91:203–219CrossRefGoogle Scholar
  124. Thorup K, Bisson I-A, Bowlin MS, Holland RA, Wingfield JC et al (2007) Evidence for a navigational map stretching across the continental U.S. in a migratory songbird. Proc Natl Acad Sci USA 104:18115–18119PubMedPubMedCentralCrossRefGoogle Scholar
  125. Thorup K, Ortvad TE, Rabøl J, Holland RA, Tøttrup AP, Wikelski M (2011) Juvenile songbirds compensate for displacement to oceanic islands during autumn migration. PLoS One 6:e17903PubMedPubMedCentralCrossRefGoogle Scholar
  126. Treiber CD, Salzer MC, Riegler J, Edelman N, Sugar C et al (2012) Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484:367–370PubMedGoogle Scholar
  127. Vardanis Y, Klaassen RHG, Strandberg R, Alerstam T (2011) Individuality in bird migration: routes and timing. Biol Lett 7:502–505PubMedPubMedCentralCrossRefGoogle Scholar
  128. Voss HU, Salgado-Commissariat D, Helekar SA (2011) Altered auditory BOLD Response to conspecific birdsong in zebra finches with stuttered syllables. PLoS One 5:e14415CrossRefGoogle Scholar
  129. Walcott C, Green RP (1974) Orientation of homing pigeons altered by a change in the direction of an applied magnetic field. Science 184:180–182PubMedCrossRefGoogle Scholar
  130. Waldvogel JA (1987) Olfactory navigation in homing pigeons: are the current models atmospherically realistic? Auk 104:369–379CrossRefGoogle Scholar
  131. Walker MM (1998) On a wing and a vector: a model for magnetic navigation by homing pigeons. J Theor Biol 192:341–349PubMedCrossRefGoogle Scholar
  132. Wallraff HG (1960) Können Grasmücken mit Hilfe des Sternenhimmels navigieren? (kritische Bearbeitung einiger Planetariumsversuche von F. Sauer). Z Tierpsychol 17:165–177CrossRefGoogle Scholar
  133. Wallraff HG (1974) Das Navigationssytem der Vögel. Oldenburg Verlag, MunichGoogle Scholar
  134. Wallraff HG (1980) Olfaction and homing in pigeons: nerve-section experiments, critique hypotheses. J Comp Physiol A 139:209–224CrossRefGoogle Scholar
  135. Wallraff HG (1981) The olfactory component of pigeon navigation: steps and analysis. J Comp Physiol 143:411–422CrossRefGoogle Scholar
  136. Wallraff HG (1982) Homing to Würzburg: an interim report on long-term analyses of pigeon navigation. In: Papi F, Wallraff HG (eds) Avian navigation. Springer Verlag, Berlin, Heidelberg, New York, pp 211–221CrossRefGoogle Scholar
  137. Wallraff HG (1999) The magnetic map of homing pigeons: an evergreen phantom. J Theor Biol 197:265–269PubMedCrossRefGoogle Scholar
  138. Wallraff HG (2000) Path integration by passively displaced homing pigeons? Anim Behav 60:F30–F36CrossRefGoogle Scholar
  139. Wallraff HG (2004) Avian olfactory navigation: its empirical foundation and conceptual state. Anim Behav 67:189–204CrossRefGoogle Scholar
  140. Wallraff HG (2005) Avian navigation: pigeon homing as a paradigm. Springer Verlag, BerlinGoogle Scholar
  141. Wallraff HG (2013) Ratios among atmospheric trace gases together with winds imply exploitable information for bird navigation: a model elucidating experimental results. Biogeosci Discuss 10:12451–12489CrossRefGoogle Scholar
  142. Wallraff HG, Andreae MO (2000) Spatial gradients in ratios of atmospheric trace gasses: a study stimulated by experiments on bird navigation. Tellus 52B:1138–1157CrossRefGoogle Scholar
  143. Wallraff HG, Kiepenheuer J, Neumann MF, Streng A (1995) Homing experiments with starlings deprived of the sense of smell. Condor 97:20–26CrossRefGoogle Scholar
  144. Wang J, Pantopoulos K (2011) Regulation of cellular ironmetabolism. Biochem J 434:365–381PubMedPubMedCentralCrossRefGoogle Scholar
  145. Weller R, Schrems O, Boddenberg A, Gäb S, Gautrois M (2000) Meridional distribution of hydroperoxides and formaldehyde in the marine boundary layer of the Atlantic (48°N–35°S) measured during the Albatross campaign. J Geophys Res 105:14401–14412CrossRefGoogle Scholar
  146. Willemoes M, Strandberg R, Klaassen RHG, Tøttrup AP, Vardanis Y et al (2014) Narrow-front loop migration in a population of the Common Cuckoo Cuculus canorus, as revealed by satellite telemetry. PLoS One 9:e83515PubMedPubMedCentralCrossRefGoogle Scholar
  147. Wiltschko R, Nehmzow U (2005) Simulating pigeon navigation. Anim Behav 69:813–826CrossRefGoogle Scholar
  148. Wiltschko W, Wiltschko R (1972) Magnetic compass of European robins. Science 176:62–64PubMedCrossRefGoogle Scholar
  149. Wiltschko W, Wiltschko R, Jahnel M (1987) The orientation behaviour of anosmic pigeons in Frankfurt aM, Germany. Anim Behav 35:1324–1333CrossRefGoogle Scholar
  150. Wiltschko W, Munro U, Ford H, Wiltschko R (1993) Red light disrupts magnetic orientation of migratory birds. Nature 364:525–527CrossRefGoogle Scholar
  151. Wiltschko W, Munro U, Beason RC, Ford H, Wiltschko R (1994) A magnetic pulse leads to a temporary deflection in the orientation of migratory birds. Experientia 50:697–700CrossRefGoogle Scholar
  152. Wiltschko W, Ford H, Munro U, Winklhofer M, Wiltschko R (2007) Magnetite-based magnetoreception: the effect of repeated pulsing on the orientation of migratory birds. J Comp Physiol A 193:515–522CrossRefGoogle Scholar
  153. Wiltschko R, Schiffner I, Fuhrmann P, Wiltschko W (2010) The role of the magnetite-based receptors in the beak in pigeon homing. Curr Biol 20:1534–1538PubMedCrossRefGoogle Scholar
  154. Wu LQ, Dickman JD (2011) Magnetoreception in an avian brain in part mediated by inner ear lagena. Curr Biol 21:418–423PubMedPubMedCentralCrossRefGoogle Scholar
  155. Wu LQ, Dickman JD (2012) Neural correlates of a magnetic sense. Science 336:1054–1057PubMedCrossRefGoogle Scholar
  156. Zapka M, Heyers D, Hein CM, Engels S, Schneider N-L et al (2009) Visual, but not trigeminal, mediation of magnetic compass information in a migratory bird. Nature 461:1274–1277PubMedCrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2015

Authors and Affiliations

  1. 1.School of Biological SciencesQueen’s University BelfastBelfastUK

Personalised recommendations