Behavioural and physiological mechanisms of Polarized light sensitivity in birds

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1565, 2011, Pages 763-771

  Muheim, Rachel ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Birds; Homing; Magnetic compass; Orientation; Polarized light; Sun compass

Indexed keywords

BEHAVIORAL RESPONSE; BIRD; CALIBRATION; EXPERIMENTAL STUDY; HOMING BEHAVIOR; ORIENTATION BEHAVIOR; PHYSIOLOGICAL RESPONSE; POLARIZATION; SENSORY SYSTEM;

AVES; INVERTEBRATA; VERTEBRATA;

EID: 79952348571     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0196     Document Type: Article

References (86)

1. Horváth, G. & Varjú, D. 2004 Polarized light in animal vision. Berlin, Germany: Springer.
2. Parkyn, D. C., Austin, J. & Hawryshyn, C. W. 2003 Acquisition of polarized light orientation in salmonids under laboratory conditions. Anim. Behav. 65, 893-904. (doi:10.1006/anbe.2003.2136) (Pubitemid 36631793)
3. Waterman, T. H. & Forward, R. B. 1970 Field evidence for polarized light sensitivity in the fish Zenarchopterus. Nature 228, 85-87. (doi:10.1038/228085a0)
4. Adler, K. & Taylor, D. H. 1973 Extraocular perception of polarized light by orienting salamanders. J. Comp. Physiol. A 87, 203-212. (doi:10.1007/BF00696042)
5. Auburn, J. S. & Taylor, D. H. 1979 Polarized light perception and orientation in larval bullfrogs, Rana catesbeiana. Anim. Behav. 27, 658-668. (doi:10.1016/0003-3472 (79) 90003-4)
6. Adler, K. & Phillips, J. B. 1985 Orientation in a desert lizard, Uma notata: time-compensated compass movement and polarotaxis. J. Comp. Physiol. A 156, 547-552. (doi:10. 1007/BF00613978)
7. Freake, M. 1999 Evidence for orientation using the e-vector direction of polarized light in the sleepy lizard, Tiliqua rugosa. J. Exp. Biol. 202, 1159-1166. (Pubitemid 29253010)
8. Brines, M. L. & Gould, J. L. 1982 Skylight polarization patterns and animal orientation. J. Exp. Biol. 96, 69-91.
9. von Frisch, K. 1949 Die Polarisation des Himmelslichtes als orientierender Faktor bei den Tänzen der Bienen. Experientia 5, 142-148. (doi:10.1007/BF02174424)
10. Wehner, R. 1976 Polarized-light navigation by insects. Sci. Am. 235, 106-115. (doi:10.1038/scientificamerican 0776-106)
11. Schmidt-Koenig, K. 1990 The sun compass. Experientia 46, 336-342. (doi:10.1007/BF01952166) (Pubitemid 120034262)
12. Wiltschko, R. 1980 Die Sonnenorientierung der Vögel. I. Die Rolle der Sonne im Orientierungssystem und die Funktionsweise des Sonnenkompass. J. Ornithol. 121, 121-143. (doi:10.1007/BF01642927)
13. Wiltschko, R. 1981 Die Sonnenorientierung der Vögel. II. Entwicklung des Sonnenkompass und sein Stellenwert im Orientierungssystem. J. Ornithol. 122, 1-22. (doi:10.1007/BF01643440)
14. Kramer, G. 1951 Eine neue Methode zur Erforschung der Zugorientierung und die bisher damit erzielten Ergebnisse. Proc. Int. Ornithol. Congr. 10, 269-280.
15. Kramer, G. 1952 Experiments on bird orientation. Ibis 94, 265-285. (doi:10.1111/j.1474-919X.1952.tb01817.x)
16. Schmidt-Koenig, K. 1958 der Einfluss experimentell veränderter Zeitschätzung auf das Heimfindevermögen der Brieftauben. Naturwissenschaften 45, 47. (doi:10. 1007/BF00635030)
17. Wiltschko, R., Walker, M. M. & Wiltschko, W. 2000 Sun-compass orientation in homing pigeons: compensation for different rates of change in azimuth? J. Exp. Biol. 203, 889-894. (Pubitemid 30194851)
18. Balda, R. P. & Wiltschko, W. 1991 Caching and recovery in scrub jays: transfer of sun-compass direction from shaded to sunny areas. Condor 93, 1020-1023. (doi:10. 2307/3247740)
19. Duff, S. J., Brownlie, L. A., Sherry, D. F. & Sangster, M. 1998 Sun compass and landmark orientation by black-capped chickadees, Parus atricapillus. J. Exp. Psychol. Anim. B 24, 243-253. (doi:10.1037/0097-7403. 24.3.243) (Pubitemid 128741620)
20. Wiltschko, W. & Balda, R. P. 1989 Sun compass orientation in seed-caching scrub jays, Aphelocoma coerulescens. J. Comp. Physiol. A 164, 717-721. (doi:10. 1007/BF00616744)
21. Wiltschko, W., Balda, R. P., Jahnel, M. & Wiltschko, R. 1999 Sun compass orientation in seed-caching corvids: its role in spatial memory. Anim. Cogn. 2, 215-221. (doi:10.1007/s100710050042)
22. Budzynski, C. A., Dyer, F. C. & Bingman, V. P. 2000 Partial experience with the arc of the sun is sufficient for all-day sun compass orientation in homing pigeons, Columba livia. J. Exp. Biol. 203, 2341-2348. (Pubitemid 30656246)
23. Chappell, J. & Guilford, T. 1995 Homing pigeons primarily use the sun compass rather than fixed directional visual cues in an open-field arena foodsearching task. Proc. R. Soc. Lond. B 260, 59-63. (doi:10.1098/rspb.1995. 0059)
24. Kramer, G. & Riese, E. 1952 Die Dressur von Brieftauben auf Kompaßrichtung im Wahlkäfig. Z. Tierpsychol. 9, 245-251. (doi:10.1111/j.1439-0310.1952.tb01852.x)
25. Kramer, G. & von Saint Paul, U. 1950 Stare, Sturnus vulgaris, lassen sich auf Himmelsrichtungen dressieren. Naturwissenschaften 37, 526-527. (doi:10.1007/BF01184829)
26. von Saint Paul, U. 1953 Nachweis der Sonnenorientierung bei nächtlich ziehenden Vögeln. Behaviour 6, 1-7. (doi:10.1163/ 156853954X00013)
27. Kramer, G. & von Saint Paul, U. 1954 Das Heimkehrvermögen gekäfigter Brieftauben. J. Ornithol. 51, 3-12.
28. von Saint Paul, U. 1956 Compass directional training of western meadowlarks, Sturnella neglecta. Auk 73, 203-210.
29. Hoffmann, K. 1954 Versuche zu der im Richtungsfinden der Vögel enthaltenen Zeitschätzung. Z. Tierpsychol. 11, 453-475. (doi:10.1111/j.1439-0310.1954.tb02169.x)
30. Keeton, W. T. 1969 Orientation by pigeons: is the Sun necessary? Science 165, 922-928. (doi:10.1126/science. 165.3896.922)
31. Schmidt-Koenig, K. & Keeton, W. T. 1977 Sun compass utilization by pigeons wearing frosted contact lenses. Auk 94, 143-145.
32. Munro, U. & Wiltschko, R. 1995 The role of skylight polarization in the orientation of a day-migrating bird species. J. Comp. Physiol. A 177, 357-362. (doi:10. 1007/BF00192424)
33. Munro, U. & Wiltschko, R. 1993 Clock-shift experiments with migratory yellow-faced honeyeaters, Lichenostomus chrysops (Meliphagidae), an Australian day-migrating bird. J. Exp. Biol. 181, 233-244.
34. Able, K. P. 1982 Skylight polarization patterns at dusk influence migratory orientation in birds. Nature 299, 550-551. (doi:10.1038/299550a0)
35. Moore, F. R. 1978 Sunset and the orientation of a nocturnal migrant bird. Nature 274, 154-156. (doi:10. 1038/274154a0) (Pubitemid 8374433)
36. Moore, F. R. 1986 Sunrise, skylight polarization, and the early morning orientation of night-migrating warblers. Condor 88, 493-498. (doi:10.2307/1368277)
37. Helbig, A. & Wiltschko, W. 1989 The skylight polarization pattern at dusk affects the orientation behaviour of blackcaps, Sylvia atricapilla. Naturwissenschaften 76, 227-229. (doi:10.1007/BF00627697)
38. Moore, F. R. & Phillips, J. B. 1988 Sunset, skylight polarization and the migratory orientation of yellow-rumped warblers, Dendroica coronata. Anim. Behav. 36, 1770-1778. (doi:10.1016/S0003-3472 (88) 80116-7)
39. Phillips, J. B. & Moore, F. R. 1992 Calibration of the sun compass by sunset polarized light patterns in a migratory bird. Behav. Ecol. Sociobiol. 31, 189-193. (doi:10.1007/BF00168646) (Pubitemid 23401725)
40. McFarland, W. N. & Munz, F. W. 1975 The visible spectrum during twilight and its implications to vision. In Light as an ecological factor: II (eds G. Evans, R. Bainbridge & O. Rackham), pp. 249-270. Oxford, UK: Blackwell Scientific Publication.
41. Helbig, A. 1990 Depolarization of natural skylight disrupts orientation of an avian nocturnal migrant. Experientia 46, 755-758. (doi:10.1007/BF01939958) (Pubitemid 20216655)
42. Helbig, A. 1991 Dusk orientation of migratory European robins, Erithacus rubecula: the role of sun-related directional information. Anim. Behav. 41, 313-322. (doi:10. 1016/S0003-3472 (05) 80483-X)
43. Phillips, J. B. & Waldvogel, J. A. 1982 Reflected light cues generate the short-term deflector-loft effect. In Avian navigation (eds F. Papi & E. Wallraff), pp. 190-202. Berlin, Germany: Springer.
44. Phillips, J. B. & Waldvogel, J. A. 1988 Celestial polarized patterns as a calibration reference for sun compass of homing pigeons. J. Theor. Biol. 131, 55-67. (doi:10. 1016/S0022-5193 (88) 80120-6)
45. Waldvogel, J. A. & Phillips, J. B. 1991 Olfactory cues perceived at the home loft are not essential for the formation of a navigational map in pigeons. J. Exp. Biol. 155, 643-660.
46. Waldvogel, J. A., Phillips, J. B. & Brown, A. I. 1988 Changes in the short-term deflector loft effect are linked to the sun compass of homing pigeons. Anim. Behav. 36, 150-158. (doi:10.1016/S0003-3472 (88) 80258-6)
47. Able, K. P. & Able, M. A. 1990 Calibration of the magnetic compass of a migratory bird by celestial rotation. Nature 347, 378-380. (doi:10.1038/347378a0) (Pubitemid 120028962)
48. Able, K. P. & Able, M. A. 1993 Daytime calibration of magnetic orientation in a migratory bird requires a view of skylight polarization. Nature 364, 523-525. (doi:10. 1038/364523a0)
49. Able, K. P. & Able, M. A. 1995 Manipulations of polarized skylight calibrate magnetic orientation in a migratory bird. J. Comp. Physiol. A 177, 351-356. (doi:10.1007/BF00192423)
50. Cochran, W. W., Mouritsen, H. & Wikelski, M. 2004 Migrating songbirds recalibrate their magnetic compass daily from twilight cues. Science 304, 405-408. (doi:10. 1126/science.1095844) (Pubitemid 38495930)
51. Muheim, R., Åkesson, S. & Phillips, J. B. 2007 Magnetic compass of migratory savannah sparrows is calibrated by skylight polarization at sunrise and sunset. J. Ornithol. 148, 485-494. (doi:10.1007/s10336-007-0187-4) (Pubitemid 350238502)
52. Muheim, R., Phillips, J. B. & Åkesson, S. 2006 Polarized light cues underlie compass calibration in migratory songbirds. Science 313, 837-839. (doi:10.1126/science. 1129709) (Pubitemid 44846385)
53. 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. J. Exp. Biol. 212, 3466-3472. (doi:10.1242/jeb.032771)
54. Muheim, R., Moore, F. R. & Phillips, J. B. 2006 Calibration of magnetic and celestial compass cues in migratory birds-a review of cue-conflict experiments. J. Exp. Biol. 209, 2-17. (doi:10.1242/jeb.01960) (Pubitemid 43163659)
55. Gaggini, V., Baldaccini, N., Spina, F. & Giunchi, D. 2010 Orientation of the pied flycatcher Ficedula hypoleuca: cue-conflict experiments during spring migration. Behav. Ecol. Sociobiol 64, 1333-1342. (doi:10.1007/s00265-010- 0948-6)
56. 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. (doi:10.1007/s10336-008-0324-8)
57. Sandberg, R. 1991 Sunset orientation of robins, Erithacus rubecula, with different fields of sky vision. Behav. Ecol. Sociobiol. 28, 77-83. (doi:10.1007/BF00180983)
58. Delius, J. D., Perchard, R. J. & Emmerton, J. 1976 Polarized light discrimination by pigeons and an electroretinographic correlate. J. Comp. Physiol. Psychol. 90, 560-571. (doi:10.1037/h0077223)
59. Kreithen, M. L. & Keeton, W. T. 1974 Detection of polarized light by the homing pigeon, Columba livia. J. Comp. Physiol. A 89, 83-92. (doi:10.1007/BF00696165)
60. Coemans, M. A. J. M., Vos Hzn, J. J. & Nuboer, J. F. W. 1990 No evidence for polarization sensitivity in the pigeon. Naturwissenschaften 77, 138-142. (doi:10.1007/BF01134480) (Pubitemid 20130819)
61. Coemans, M. A. J. M., Vos Hzn, J. J. & Nuboer, J. F. W. 1994 The orientation of the e-vector of linearly polarized light does not affect the behaviour of the pigeon, Columba livia. J. Exp. Biol. 191, 107-123.
62. Montgomery, K. C. & Heinemann, E. G. 1952 Concerning the ability of homing pigeons to discriminate patterns of polarized light. Science 116, 454-456. (doi:10.1126/science.116.3017.454)
63. Vos Hzn, J., Coemans, M. & Nuboer, J. 1995 No evidence for polarization sensitivity in the pigeon electroretinogram. J. Exp. Biol. 198, 325-335.
64. Greenwood, V. J., Smith, E. L., Church, S. C. & Partridge, J. C. 2003 Behavioural investigation of polarisation sensitivity in the Japanese quail, Coturnix coturnix japonica, and the European starling, Sturnus vulgaris. J. Exp. Biol. 206, 3201-3210. (doi:10.1242/jeb.00537) (Pubitemid 37181418)
65. Cameron, D. A. & Pugh, E. N. 1991 Double cones as a basis for a new type of polarization vision in vertebrates. Nature 353, 161-164. (doi:10.1038/353161a0) (Pubitemid 21912480)
66. Young, S. R. & Martin, G. R. 1984 Optics of retinal oil droplets: a model of light collection and polarization detection in the avian retina. Vis. Res. 24, 129-137. (doi:10.1016/0042-6989 (84) 90098-1) (Pubitemid 14181469)
67. Coughlin, D. J. & Hawryshyn, C. W. 1995 A cellular basis for polarized-light vision in rainbow trout. J. Comp. Physiol. A 176, 261-272. (doi:10.1007/BF00239928)
68. Hawryshyn, C. W. & McFarland, W. N. 1987 Cone photoreceptor mechanisms and the detection of polarized light in fish. J. Comp. Physiol. A 160, 459-465. (doi:10.1007/BF00615079)
69. Roberts, N. W. & Needham, M. 2007 A mechanism of polarized light sensitivity in cone photoreceptors of the goldfish, Carassius auratus. Biophys. J. 93, 3241-3248. (doi:10.1529/biophysj.107.112292) (Pubitemid 350097114)
70. Flamarique, I. N., Hawryshyn, C. W. & Hárosi, F. I. 1998 Double-cone internal reflection as a basis for polarization detection in fish. J. Opt. Soc. Am. A 15, 349-358. (doi:10.1364/JOSAA.15.000349) (Pubitemid 128567490)
71. Hart, N. S. & Hunt, D. M. 2007 Avian visual pigments: characteristics, spectral tuning, and evolution. Am. Nat. 169, S7-S26. (doi:10.1086/510141) (Pubitemid 46094996)
72. Engström, K. 1958 On the cone mosaic in the retina of Parus major. Acta Zool. 39, 65-69. (doi:10.1111/j.1463-6395.1958.tb00523.x)
73. Kram, Y. A., Mantey, S. & Corbo, J. C. 2010 Avian cone photoreceptors tile the retina as five independent, self-organizing mosaics. PLoS ONE 5, e8992. (doi:10. 1371/journal.pone.0008992)
74. Morris, V. B. 1970 Symmetry in a receptor mosaic demonstrated in the chick from the frequencies, spacing and arrangement of the types of retinal receptor. J. Comp. Neurol. 140, 359-397. (doi:10.1002/cne.901400308)
75. Phillips, J. B., Deutschlander, M. E., Freake, M. J. & Borland, S. C. 2001 The role of extraocular photoreceptors in newt magnetic compass orientation: parallels between light-dependent magnetoreception and polarized light detection. J. Exp. Biol. 204, 2543-2552. (Pubitemid 34869480)
76. Wiltschko, W. & Wiltschko, R. 2002 Magnetic orientation in birds and its physiological basis. Naturwissenschaften 89, 445-452. (doi:10.1007/s00114- 002-0356-5) (Pubitemid 35346981)
77. Muheim, R., Bäckman, J. & Åkesson, S. 2002 Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light. J. Exp. Biol. 205, 3845-3856. (Pubitemid 36059037)
78. Wiltschko, R., Stapput, K., Thalau, P. & Wiltschko, W. 2010 Directional orientation of birds by the magnetic field under different light conditions. J. R. Soc. Interface 7, S163-S177. (doi:10.1098/rsif.2009.0367. focus)
79. Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. 2003 Magnetic orientation in birds: non-compass responses under monochromatic light of increased intensity. Proc. R. Soc. Lond. B 270, 2133-2140. (doi:10. 1098/rspb.2003.2476) (Pubitemid 37289879)
80. Ritz, T., Adem, S. & Schulten, K. 2000 A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707-718. (doi:10.1016/S0006-3495 (00) 76629-X) (Pubitemid 30211829)
81. Phillips, J. B., Jorge, P. E. & Muheim, R. 2010 Lightdependent magnetic compass orientation in amphibians and insects: candidate receptors and candidate molecular mechanisms. J. R. Soc. Interface 7, S241-S256. (doi:10. 1098/rsif.2009.0459.focus)
82. Parkyn, D. C. & Hawryshyn, C. W. 1993 Polarized-light sensitivity in rainbow trout, Oncorhynchus mykiss: characterizationfrom multi-unit responses inthe optic nerve. J. Comp. Physiol. A 172, 493-500. (doi:10.1007/BF00213531)
83. Ramsden, S. D., Anderson, L., Mussi, M., Kamermans, M. & Hawryshyn, C. W. 2008 Retinal processing and opponent mechanisms mediating ultraviolet polarization sensitivity in rainbow trout, Oncorhynchus mykiss. J. Exp. Biol. 211, 1376-1385. (doi:10.1242/jeb.015941) (Pubitemid 351954820)
84. Phillips, J. B. & Borland, S. C. 1992 Behavioural evidence for use of light-dependent magnetoreception mechanism by a vertebrate. Nature 359, 142-144. (doi:10.1038/359142a0)
85. Wehner, R. 1987 'Matched filters'-neural models of the external world. J. Comp. Physiol. A 161, 511-531. (doi:10.1007/BF00603659)
86. Phillips, J. B., Muheim, R. & Jorge, P. E. 2010 A behavioral perspective on the biophysics of the light-dependent magnetic compass: a link between directional and spatial perception? J. Exp. Biol. 213, 3247-3255. (doi:10.1242/jeb.020772)