Restricted access
Articles
ArticlesAn unsuccessful attempt to elicit orientation responses to linearly polarized light in hatchling loggerhead sea turtles (Caretta caretta)
Published:12 March 2011https://doi.org/10.1098/rstb.2010.0212
Abstract
Sea turtles undertake long migrations in the open ocean, during which they rely at least partly on magnetic cues for navigation. In principle, sensitivity to polarized light might be an additional sensory capability that aids navigation. Furthermore, polarization sensitivity has been linked to ultraviolet (UV) light perception which is present in sea turtles. Here, we tested the ability of hatchling loggerheads (Caretta caretta) to maintain a swimming direction in the presence of broad-spectrum polarized light. At the start of each trial, hatchling turtles, with their magnetic sense temporarily impaired by magnets, successfully established a steady course towards a light-emitting diode (LED) light source while the polarized light field was present. When the LED was removed, however, hatchlings failed to maintain a steady swimming direction, even though the polarized light field remained. Our results have failed to provide evidence for polarized light perception in young sea turtles and suggest that alternative cues guide the initial migration offshore.
References
- 1
- 2
Salmon M., Wyneken J., Fritz E.& Lucas M. . 1992Seafinding by hatchling sea turtles: role of brightness, silhouette and beach slope as orientation cues. Behaviour 122, 56–77.doi:10.1163/156853992X00309 (doi:10.1163/156853992X00309). Crossref, ISI, Google Scholar - 3
Lohmann K. J., Swartz A. W.& Lohmann C. M. F. . 1995Perception of ocean wave direction by sea turtles. J. Exp. Biol. 198, 1079–1085. Crossref, PubMed, ISI, Google Scholar - 4
Lohmann K. J. . 1991Magnetic orientation by hatchling loggerhead sea turtles (Caretta caretta). J. Exp. Biol. 155, 37–49. Crossref, PubMed, ISI, Google Scholar - 5
Lohmann K. J. . 1993Magnetic compass orientation. Nature 362, 703.doi:10.1038/362703a0 (doi:10.1038/362703a0). Crossref, PubMed, ISI, Google Scholar - 6
Lohmann K. J.& Lohmann C. M. . 1996Orientation and open-sea navigation in sea turtles. J. Exp. Biol. 199, 73–81. Crossref, PubMed, ISI, Google Scholar - 7
Horváth G.& Varjú D. . 2004Polarized light in animal vision. Polarization patterns in nature.Berlin, Germany: Springer. Crossref, Google Scholar - 8
Moody M. F.& Parriss J. R. . 1960The visual system of Octopus: (2) Discrimination of polarized light by Octopus. Nature 186, 839–840.doi:10.1038/186839a0 (doi:10.1038/186839a0). Crossref, PubMed, ISI, Google Scholar - 9
Shashar N., Hanlon R. T.& Petz A. D. . 1998Polarization vision helps detect transparent prey. Nature 393, 222–223.doi:10.1038/30380 (doi:10.1038/30380). Crossref, PubMed, ISI, Google Scholar - 10
Shashar N., Rutledge P. S.& Cronin T. W. . 1996Polarization vision in cuttlefish—a concealed communication channel?J. Exp. Biol. 199, 2077–2084. Crossref, PubMed, ISI, Google Scholar - 11
Marshall N. J. . 1988A unique color and polarization vision system in mantis shrimps. Nature 213, 893–894. Google Scholar - 12
Marshall N. J., Land M. F., King C. A.& Cronin T. W. . 1991The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). I. Compound eye structure: the detection of polarized light. Phil. Trans. R. Soc. Lond. B 334, 33–56.doi:10.1098/rstb.1991.0096 (doi:10.1098/rstb.1991.0096). Link, ISI, Google Scholar - 13
Dacke M., Nilsson D. E., Scholtz C. H., Byrne M.& Warrant E. J. . 2003Insect orientation to polarized moonlight. Nature 424, 33.doi:10.1038/424033a (doi:10.1038/424033a). Crossref, PubMed, ISI, Google Scholar - 14
Kelber A., Thunell C.& Arikawa K. . 2001Polarization-dependent color vision in Papilio butterflies. J. Exp. Biol. 204, 2469–2480. Crossref, PubMed, ISI, Google Scholar - 15
Rossel S. . 1989Polarization sensitivity in compound eyes. Facets of vision (eds, Stavenga D. G.& Hardie R. C. ), pp. 298–316. Berlin, Germany: Springer. Crossref, Google Scholar - 16
Rossel S.& Wehner R. . 1984How bees analyse the polarization patterns in the sky. J. Comp. Physiol. A 154, 607–615.doi:10.1007/BF01350213 (doi:10.1007/BF01350213). Crossref, ISI, Google Scholar - 17
Sweeney A., Jiggins C.& Johnsen S. . 2003Polarized light as a butterfly mating signal. Nature 423, 31–32.doi:10.1038/423031a (doi:10.1038/423031a). Crossref, PubMed, ISI, Google Scholar - 18
Wehner R. . 1989Neurobiology of polarization vision. Trends Neurosci. 12, 353–359.doi:10.1016/0166-2236(89)90043-X (doi:10.1016/0166-2236(89)90043-X). Crossref, PubMed, ISI, Google Scholar - 19
Wehner R. . 2001Polarization vision—a uniform sensory capacity?J. Exp. Biol. 204, 2589–2596. Crossref, PubMed, ISI, Google Scholar - 20
Johnsen S. . 1994Extraocular sensitivity to polarized light in an echinoderm. J. Exp. Biol. 195, 281–291. Crossref, PubMed, ISI, Google Scholar - 21
Auburn J. S.& Taylor D. J. . 1979Polarized light perception and orientation in larval bullfrogs Rana catesbeiana. Anim. Behav. 27, 658–688.doi:10.1016/0003-3472(79)90003-4 (doi:10.1016/0003-3472(79)90003-4). Crossref, ISI, Google Scholar - 22
Taylor D.& Adler K. . 1973Spatial orientation by salamanders using plane-polarized light. Science 181, 285–287.doi:10.1126/science.181.4096.285 (doi:10.1126/science.181.4096.285). Crossref, PubMed, ISI, Google Scholar - 23
Sabbah S., Lerner A., Erlick C.& Shashar N. . 2005Under water polarization vision: a physical examination. Recent research developments in experimental and theoretical biology (ed.& Pandalai S. G. ), pp. 123–176. Kerala, India: Transworld Research Network. Google Scholar - 24
Kreithen M. L.& Keeton W. T. . 1974Detection of polarized light by the homing pigeon, Columba livia. J. Comp. Physiol. 89, 83–92.doi:10.1007/BF00696165 (doi:10.1007/BF00696165). Crossref, ISI, Google Scholar - 25
Muheim R., Phillips J. B.& Akesson S. . 2006Polarized light cues undelie compass calibration in migratory songbirds. Science 313, 837–839.doi:10.1126/science.1129709 (doi:10.1126/science.1129709). Crossref, PubMed, ISI, Google Scholar - 26
Phillips J. B.& Waldvogel J. A. . 1988Celestial polarized light 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 (doi:10.1016/S0022-5193(88)80120-6). Crossref, ISI, Google Scholar - 27
Coemans M.& Vos J. . 1992On the perception of polarized light by the homing pigeon.Utrecht, Nederlands: Utrecht University. Google Scholar - 28
Hzn J., Coemans M.& Nuboer J. . 1995No evidence for polarization sensitivity in the pigeon electroretinogram. J. Exp. Biol. 198, 325–335. Crossref, PubMed, ISI, Google Scholar - 29
Rossel S. . 1993Navigation by bees using polarized skylight. Comp. Biochem. Physiol. 104, 695–708.doi:10.1016/0300-9629(93)90146-U (doi:10.1016/0300-9629(93)90146-U). Crossref, Google Scholar - 30
Rossel S.& Wehner R. . 1986Polarization vision in bees. Nature 323, 128–131.doi:10.1038/323128a0 (doi:10.1038/323128a0). Crossref, ISI, Google Scholar - 31
Shashar N., Sabbah S.& Aharoni N. . 2005Migrating locusts can detect polarized reflections to avoid flying over the sea. Biol. Lett. 1, 472–475.doi:10.1098/rsbl.2005.0334 (doi:10.1098/rsbl.2005.0334). Link, ISI, Google Scholar - 32
Wehner R.& Müller M. . 2006The significance of direct sunlight and polarized skylight in the ant's celestial system of navigation. Proc. Natl Acad. Sci. USA 103, 12 575–12 579.doi:10.1073/pnas.0604430103 (doi:10.1073/pnas.0604430103). Crossref, ISI, Google Scholar - 33
Liebman P. A.& Granda A. M. . 1971Microspectrophotometric measurements of visual pigments in two species of turtle, Pseudemys scripta and Chelonia mydas. Vis. Res. 11, 105–114.doi:10.1016/0042-6989(71)90227-6 (doi:10.1016/0042-6989(71)90227-6). Crossref, PubMed, ISI, Google Scholar - 34
Liebman P. A.& Granda A. M. . 1975Super dense carotenoid spectra resolved in single cone oil droplets. Nature 253, 370–372.doi:10.1038/253370a0 (doi:10.1038/253370a0). Crossref, PubMed, ISI, Google Scholar - 35
Mäthger L. M., Litherland L.& Fritsches K. A. . 2007An anatomical study of the visual capabilities of the green turtle, Chelonia mydas. Copeia 2007, 169–179.doi:10.1643/0045-8511(2007)7[169:AASOTV]2.0.CO;2 (doi:10.1643/0045-8511(2007)7[169:AASOTV]2.0.CO;2). Crossref, Google Scholar - 36
Horch K. W., Gocke J. P., Salmon M.& Forward R. B. . 2008Visual spectral sensitivity of hatchling loggerhead (Caretta caretta L.) and leatherback (Dermochelys coriacea L.) sea turtles, as determined by single-flash electroretinography. Mar. Freshw. Behav. Physiol. 41, 107–119.doi:10.1080/10236240802106556 (doi:10.1080/10236240802106556). Crossref, ISI, Google Scholar - 37
Witherington B. E.& Bjorndal K. A. . 1991Influences of wavelength and intensity on hatchling sea turtle phototaxis: implications for sea-finding behaviour. Copeia 4, 1060–1069.doi:10.2307/1446101 (doi:10.2307/1446101). Crossref, Google Scholar - 38
Hawryshyn C. W. . 2000Ultraviolet polarization vision in fishes: possible mechanisms for coding e-vector. Phil. Trans. R. Soc. Lond. B 355, 1187–1190.doi:10.1098/rstb.2000.0664 (doi:10.1098/rstb.2000.0664). Link, ISI, Google Scholar - 39
Hawryshyn C. W.& McFarland W. N. . 1987Cone photoreceptor mechanisms and the detection of polarized light in fish. J. Comp. Physiol. A 160, 459–465.doi:10.1007/BF00615079 (doi:10.1007/BF00615079). Crossref, ISI, Google Scholar - 40
Irwin W. P.& Lohmann K. J. . 2003Magnet-induced disorientation in hatchling loggerhead sea turtles. J. Exp. Biol. 206, 497–501.doi:10.1242/jeb.00108 (doi:10.1242/jeb.00108). Crossref, PubMed, ISI, Google Scholar - 41
Salmon M.& Wyneken J. . 1987Orientation and swimming behavior of hatchling loggerhead turtles Caretta caretta during their offshore migration. J. Exp. Mar. Biol. Ecol. 109, 137–153.doi:10.1016/0022-0981(87)90012-8 (doi:10.1016/0022-0981(87)90012-8). Crossref, ISI, Google Scholar - 42
Dacke M., Nordström P.& Scholtz C. H. . 2003Twilight orientation to polarised light in the crepuscular dung beetle Scarabaeus zambesianus. J. Exp. Biol. 206, 1535–1543.doi:10.1242/jeb.00289 (doi:10.1242/jeb.00289). Crossref, PubMed, ISI, Google Scholar - 43
Ehrenfeld E. W.& Carr A. . 1967The role of vision in the sea-finding orientation of the green turtle (Chelonia mydas). Anim. Behav. 15, 25–36.doi:10.1016/S0003-3472(67)80007-1 (doi:10.1016/S0003-3472(67)80007-1). Crossref, PubMed, ISI, Google Scholar - 44
Hawryshyn C. W.& McFarland W. N. . 1987Cone photoreceptor mechanisms and the detection of polarized light in fish. J. Comp. Physiol. A 160, 459–465.doi:10.1007/BF00615079 (doi:10.1007/BF00615079). Crossref, ISI, Google Scholar - 45
Mussi M., Haimberger T. J.& Hawryshyn C. W. . 2005Behavioural discrimination of polarized light in the damselfish Chromis viridis (family Pomacentridae). J. Exp. Biol. 208, 3037–3046.doi:10.1242/jeb.01750 (doi:10.1242/jeb.01750). Crossref, PubMed, ISI, Google Scholar - 46
Parkyn D. C.& Hawryshyn C. W. . 1993Polarized-light sensitivity in rainbow trout (Oncorhynchus mykiss): characterization from multi-unit responses in the optic nerve. J. Comp. Physiol. A 172, 493–500.doi:10.1007/BF00213531 (doi:10.1007/BF00213531). Crossref, ISI, Google Scholar - 47
Zigman S. . 1971Eye lens color: formation and function. Science 171, 807–809.doi:10.1126/science.171.3973.807 (doi:10.1126/science.171.3973.807). Crossref, PubMed, ISI, Google Scholar - 48
Fritsches K. A., Partridge J., Pettigrew J. D.& Marshall N. J. . 2000Colour vision in billfish. Phil. Trans. R. Soc. Lond. B 355, 1253–1256.doi:10.1098/rstb.2000.0678 (doi:10.1098/rstb.2000.0678). Link, ISI, Google Scholar - 49
Siebeck U. E.& Marshall N. J. . 2000Transmission of ocular media in labrid fishes. Phil. Trans. R. Soc. Lond. B 355, 1257–1261.doi:10.1098/rstb.2000.0679 (doi:10.1098/rstb.2000.0679). Link, ISI, Google Scholar - 50
Losey G. S., Cronin T. W., Goldsmith T. H., Hyde D., Marshall N. J.& McFarland W. N. . 1999The UV visual world of fishes: a review. J. Fish Biol. 54, 921–943.doi:10.1111/j.1095-8649.1999.tb00848.x (doi:10.1111/j.1095-8649.1999.tb00848.x). Crossref, ISI, Google Scholar - 51
Coughlin D. J.& Hawryshyn C. W. . 1995A cellular basis for polarized-light vision in rainbow-trout. J. Comp. Physiol. A 176, 261–272.doi:10.1007/BF00239928 (doi:10.1007/BF00239928). Crossref, ISI, Google Scholar - 52
Lohmann K. J.& Lohmann C. M. F. . 2003Orientation mechanisms of hatchling loggerhead turtles (Caretta caretta). Biology and conservation of loggerhead sea turtles (eds, Bolten A.& Witherington B. ), pp. 44–62. Washington, DC: Smithsonian Institute Press. Google Scholar - 53
Bowmaker J. K. . 1990Visual pigments of fish. The visual system of fish (eds, Douglas R. H.& Djamgoz M. B. A. ), pp. 81–104. London, UK: Chapman and Hall. Crossref, Google Scholar - 54
Wiltschko R. . 1983The ontogeny of orientation in young homing pigeons. Comp. Biochem. Physiol A 76, 701–708.doi:10.1016/0300-9629(83)90131-7 (doi:10.1016/0300-9629(83)90131-7). Crossref, ISI, Google Scholar
