Polarization sensitivity as a contrast enhancer in pelagic predators: Lessons from in situ polarization imaging of transparent zooplankton

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1565, 2011, Pages 655-670

  Johnsen, Sönke ^a   Marshall, N Justin ^b   Widder, Edith A ^c  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c Ocean Research & Conservation Association Inc   (United States)

Author keywords

Birefringence; Camouflage; Polarization sensitivity; Transparency; Visual predation; Zooplankton

Indexed keywords

BIREFRINGENCE; IMAGING METHOD; INVERTEBRATE; IRRADIANCE; MICRONEKTON; PELAGIC ENVIRONMENT; POLARIZATION; PREDATION; TRANSPARENCY; UNDERWATER ENVIRONMENT; VISIBILITY; VISUAL CUE; ZOOPLANKTON;

ATLANTIC OCEAN; AUSTRALIA; CORAL SEA; GREAT BARRIER REEF; GULF OF MEXICO; PACIFIC OCEAN; QUEENSLAND;

ANIMALIA; CEPHALOPODA; CTENOPHORA (COELENTERATES); GASTROPODA; SALPIDA;

EID: 79952340676     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0193     Document Type: Article

References (64)

1. Hawryshyn, C. W. 2000 Ultraviolet 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)
2. Waterman, T. H. 1988 Polarization of marine light fields and animal orientation. SPIE 925, 431-437.
3. Wehner, R. & Labhart, T. 2006 Polarization vision. In Invertebrate vision (eds E. J. Warrant & D. E. Nilsson), pp. 291-348. Cambridge, UK:Cambridge University Press.
4. Goddard, S. M. & Forward, R. B. J. 1991 The role of the underwater polarized light pattern, in sun compass navigation of the grass shrimp Palaemonetes vulgaris L. J. Comp. Physiol. A 169, 479-491. (doi:10.1007/ BF00197660)
5. Rossel, S. 1993 Navigation by bees using polarized skylight. Comp. Biochem. Phys. A 104, 695-708. (doi:10.1016/0300-9629 (93) 90146-U) (Pubitemid 23094352)
6. Wehner, R. 1976 Polarized-light navigation by insects. Sci. Am. 235, 106-115. (doi:10.1038/scientificamerican 0776-106)
7. Chiou, T.-H., Kleinlogel, S., Cronin, T. W., Caldwell, R., Loeffler, B., Siddiqi, A., Goldizen, A. & Marshall, N. J. 2008 Circular polarization vision in a stomatopod crustacean. Curr. Biol. 18, 429-434. (doi:10.1016/j. cub.2008.02.066)
8. Cronin, T. W., Shashar, N., Caldwell, R. L., Marshall, J., Cheroske, A. G. & Chiou, T. H. 2003 Polarization vision and its role in biological signalling. Integr. Comp. Biol. 43, 549-558. (doi:10.1093/icb/43.4.549) (Pubitemid 38335317)
9. Shashar, N., Rutledge, P. & Cronin, T. W. 1996 Polarization vision in cuttlefish-a concealed communication channel? J. Exp. Biol. 199, 2077-2084. (Pubitemid 26352515)
10. Horváth, G. & Kriska, G. 2008 Polarization vision in aquatic insects and ecological traps for polarotactic insects. In Aquatic insects: challenges to populations (eds J. Lancaster & R. A. Briers), pp. 204-229. Wallingford, UK: CAB International Publishing.
11. Horváth, G., Kriska, G., Malik, P. & Robertson, B. 2009 Polarized light pollution: a new kind of ecological photopollution. Front. Ecol. Environ. 7, 317-325. (doi:10. 1890/080129)
12. Schwind, R. 1991 Polarization vision in water insects and insects living on a moist substrate. J. Comp. Physiol. A 169, 531-540. (doi:10.1007/BF00193544)
13. Schwind, R. 1995 Spectral regions in which aquatic insects see reflected polarized light. J. Comp. Physiol. A 177, 439-448. (doi:10.1007/BF00187480)
14. Lythgoe, J. N. & Hemmings, C. C. 1967 Polarized light and underwater vision. Nature 213, 893-894. (doi:10. 1038/213893a0)
15. Shashar, N., Hanlon, R. T. & Petz, A. 1998 Polarization vision helps detect transparent prey. Nature 393, 222-223. (doi:10.1038/30380) (Pubitemid 28261711)
16. Shashar, N., Hagan, R., Boal, J. G. & Hanlon, R. T. 2000 Cuttlefish use polarization sensitivity in predation on silvery fish. Vision Res. 40, 71-75. (doi:10.1016/S0042-6989 (99) 00158-3)
17. Denton, E. J. 1970 On the organization of reflecting structures in some marine animals. Phil. Trans. R. Soc. Lond. B 258, 285-313. (doi:10.1098/rstb. 1970.0037)
18. Herring, P. J. 1994 Reflective systems in aquatic animals. Comp. Biochem. Physiol. A 109, 513-546. (doi:10.1016/0300-9629 (94) 90192-9) (Pubitemid 24335320)
19. Johnsen, S. & Widder, E. A. 1998 The transparency and visibility of gelatinous zooplankton from the north west Atlantic and Gulf of Mexico. Biol. Bull. 195, 337-348. (doi:10.2307/1543145) (Pubitemid 29049794)
20. Johnsen, S. 2001 Hidden in plain sight: the ecology and physiology of organismal transparency. Biol. Bull. 201, 301-318. (doi:10.2307/1543609) (Pubitemid 34057127)
21. Johnsen, S. & Sosik, H. M. 2003 Cryptic coloration and mirrored sides as camouflage strategies in near-surface pelagic habitats: implications for foraging and predator avoidance. Limnol. Oceanogr. 48, 1277-1288. (doi:10. 4319/lo.2003.48.3.1277) (Pubitemid 36631969)
22. McFall-Ngai, M. J. 1990 Crypsis in the pelagic environment. Am. Zool. 30, 175-188.
23. Briggs, R. O. & Hatchett, G. L. 1965 Techniques for improving underwater visibility with video equipment. Ocean Sci. Eng. 1, 1284-1308.
24. Gilbert, G. D. & Pernicka, J. C. 1966 Improvement of underwater visibility by reduction of backscatter with a circular polarization technique. Appl. Opt. 6, 741-746. (doi:10.1364/AO.6.000741)
25. Nathan, A. M. 1957 A polarization technique for seeing through fogs with active optical systems. Technical report 362. 01. New York University, New York.
26. Schechner, Y. Y., Narasimhan, S. G. & Nayar, S. K. 2003 Polarization-based vision through haze. Appl. Opt. 42, 511-525. (doi:10.1364/AO.42.000511)
27. Schechner, Y. Y. & Karpel, N. 2005 Recovery of underwater visibility and structure by polarization analysis. IEEE J. Ocean Eng. 30, 570-587. (doi:10.1109/JOE. 2005.850871) (Pubitemid 43264147)
28. Horváth, G. & Varjú, D. 2004 Polarized light in animal vision-polarization patterns in nature. New York, NY: Springer.
29. Sweeney, A. M., Jiggins, C. & Johnsen, S. 2003 Polarized light as a butterfly mating signal. Nature 423, 31-32. (doi:10.1038/423031a) (Pubitemid 36569575)
30. Duntley, S. Q. 1952 The visibility of submerged objects. Final report to Office of Naval Research, Washington, DC, USA.
31. Mertens, L. E. 1970 In-water photography: theory and practice. New York, NY: John Wiley & Sons.
32. Johnsen, S. 2002 Cryptic and conspicuous coloration in the pelagic environment. Proc. R. Soc. Lond. B 269, 243-256. (doi:10.1098/rspb.2001.1855) (Pubitemid 34161031)
33. Shashar, N., Sabbah, S. & Cronin, T. W. 2004 Transmission of linearly polarized light in seawater: implications for polarization signaling. J. Exp. Biol. 207, 3619-3628. (doi:10.1242/jeb.01187) (Pubitemid 39384816)
34. Haddock, S. H. D. & Heine, J. N. 2005 Scientific Blue-Water diving. La Jolla, CA: California Sea Grant College Program.
35. Hamner, W. M., Madin, L. P., Alldredge, A. L., Gilmer, R. W. & Hamner, P. P. 1975 Underwater observations of gelatinous zooplankton: sampling problems, feeding biology, and behaviour. Limnol. Oceanogr. 20, 907-917. (doi:10.4319/lo.1975.20.6.0907)
36. Wolff, L. B. & Andreou, A. G. 1995 Polarization camera sensors. Image Vis. Comp. 13, 497-510. (doi:10.1016/0262-8856 (95) 94383-B)
37. Bernard, G. D. & Wehner, R. 1977 Functional similarities between polarization vision and colour vision. Vision Res. 17, 1019-1028. (doi:10.1016/0042-6989 (77) 90005-0) (Pubitemid 8209912)
38. Jacques, S. L., Roman, J. R. & Lee, K. 2000 Imaging superficial tissues with polarized light. Laser Surg. Med. 26, 119-129. (doi:10.1002/(SICI) 1096-9101 (2000) 26:2<119::AID-LSM3>3.0. CO;2-Y) (Pubitemid 30118372)
39. Cronin, T. W. & Shashar, N. 2001 The linearly polarized light field in clear, tropical marine waters: spatial and temporal variation of light intensity, degree of polarization and e-vector angle. J. Exp. Biol. 204, 2461-2467. (Pubitemid 34869471)
40. Cronin, T. W. & Marshall, J. 2011 Patterns and properties of polarized light in air and water. Phil. Trans. R. Soc. B 366, 619-626. (doi:10.1098/rstb.2010.0201)
41. Ivanoff, A. & Waterman, T. H. 1958 Elliptical polarization of submarine illumination. J. Mar. Res. 16, 255-282.
42. Ivanoff, A. & Waterman, T. H. 1958 Factors, mainly depth and wavelength, affecting the degree of underwater light polarization. J. Mar. Res. 16, 283-307.
43. Michiels, N. et al. 2008 Red fluorescence in reef fish: a novel signalling mechanism? BMC Ecol. 8, 16. (doi:10. 1186/1472-6785-8-16)
44. Cuthill, I. C., Bennett, A. T. D., Partridge, J. C. & Maier, E. J. 1999 Plumage reflectance and the objective assessment of avian sexual dichromatism. Am. Nat. 160, 183-200. (doi:10.1086/303160) (Pubitemid 29139435)
45. Siebeck, U. E., Parker, A. N., Sprenger, D., Mäthger, L. M. & Wallis, G. 2010 A species of reef fish that uses ultraviolet patterns for covert face recognition. Curr. Biol. 20, 407-410. (doi:10.1016/j.cub.2009.12.047)
46. Arnold, K. E., Owens, A. P. F. & Marshall, N. J. 2002 Fluorescent signalling in parrots. Science 295, 92-93. (doi:10.1126/science.295.5552.92) (Pubitemid 34052350)
47. Gagnon, Y. L., Shashar, N., Warrant, E. J. & Johnsen, S. 2007 Light scattering from pelagic zooplankton: measurements at different angles and modeling corresponding sighting distances. J. Exp. Biol. 210, 3728-3735. (doi:10.1242/jeb.003251) (Pubitemid 350206240)
48. Denton, E. J., Gilpin-Brown, J. B. & Wright, P. G. 1972 The angular distribution of the light produced by some mesopelagic fish in relation to their camouflage. Proc. R. Soc. Lond. B 182, 145-158. (doi:10.1098/rspb. 1972.0071)
49. Marshall, N. J., Land, M. F., King, C. A. & Cronin, T. W. 1991 The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). I. Compound eye structure: the detection of polarised light. Phil. Trans. R. Soc. Lond. B 334, 33-56. (doi:10.1098/rstb.1991.0096)
50. Marshall, N. J., Kent, J. & Cronin, T. W. 1999 Visual adaptations in crustaceans. In Adaptive mechanisms in the ecology of vision (eds S. N. Archer, M. B. A. Djamgoz, E. Lowe, J. C. Partridge & S. Vallerga), pp. 285-328. London, UK: Kluwer Academic.
51. Talbot, C. M. & Marshall, J. N. 2011 The retinal topography of three species of coleoid cephalopod: significance for perception of polarized light. Phil. Trans. R. Soc. B 366, 724-733. (doi:10.1098/rstb.2010.0254)
52. Yemelyanov, K., Lin, S. S., Pugh Jr, E. N. & Engheta, N. 2006 Adaptive algorithms for 2-channel polarization sensing under various polarization statistics with nonuniform distributions. Appl. Opt. 45, 5504-5520. (doi:10.1364/AO.45.005504) (Pubitemid 44562641)
53. Glantz, R. M. 1996 Polarization sensitivity in crayfish lamina monopolar neurons. J. Comp. Physiol. A 178, 413-425. (doi:10.1007/BF00193978)
54. Sabra, R. & Glantz, R. M. 1985 Polarisation sensitivity of crayfish photoreceptors is correlated with their termination sites in the lamina ganglionaris. J. Comp. Physiol. 156, 315-318. (doi:10.1007/BF00610724)
55. Saidel, W. M., Lettvin, J. Y. & MacNichol, E. F. J. 1983 Processing of polarized light by squid photoreceptors. Nature 304, 534-536. (doi:10.1038/304534a0) (Pubitemid 13026949)
56. Hawryshyn, C. W. 1992 Polarization vision in fish. Am. Sci. 80, 164-175.
57. Kamermans, M. & Hawryshyn, C. 2011 Teleost polarisation vision: how it might work and what it might be good for. Phil. Trans. R. Soc. B 366, 742-756. (doi:10. 1098/rstb.2010.0211)
58. Muheim, R. 2011 Behavioural and physiological mechanisms of polarized light sensitivity in birds. Phil. Trans. R. Soc. B 366, 763-771. (doi:10.1098/rstb.2010.0196)
59. Bicout, D., Brosseau, C., Martinez, A. S. & Schmitt, J. M. 1994 Depolarization of multiple scattered waves by spherical diffusers: influence of the size parameter. Phys. Rev. E 49, 1767-1770. (doi:10.1103/PhysRevE.49.1767)
60. Morgan, S. P., Khong, M. P. & Somekh, M. G. 1997 Effects of polarization state and scatterer concentration on optical imaging through scattering media. Appl. Opt. 36, 1560-1565. (doi:10.1364/AO.36.001560) (Pubitemid 127638574)
61. Douglas, R. H. & Hawryshyn, C. W. 1990 Behavioural studies of fish vision: an analysis of visual capabilities. In The visual system of fish (eds R. H. Douglas & M. B. A. Djamgoz), pp. 373-418. New York, NY: Chapman and Hall.
62. Dacke, M., Nilsson, D.-E., Scholtz, C. H., Byrne, M. & Warrant, E. J. 2003 Animal behaviour: insect orientation to polarized moonlight. Nature 424, 33. (doi:10.1038/424033a) (Pubitemid 36834830)
63. Labhart, T. 1996 How polarization-sensitive interneurons perform at low degrees of polarization. J. Exp. Biol. 199, 1467-1475. (Pubitemid 26263616)
64. Pignatelli, V., Temple, S. E., Chiou, T.-H., Roberts, N. W., Collin, S. P. & Marshall, N. J. 2011 Behavioural relevance of polarization sensitivity as a target detection mechanism in cephalopods and fishes. Phil. Trans. R. Soc. B 366, 734-741. (doi:10.1098/rstb.2010. 0204)