A spitting image: Specializations in archerfish eyes for vision at the interface between air and water

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1694, 2010, Pages 2607-2615

  Temple, Shelby ^a   Hart, Nathan S ^a,b   Marshall, N Justin ^a   Collin, Shaun P ^a,b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Acuity; Chromophore; Colour vision; Fish; Opsin; Toxotes chatareus

Indexed keywords

ABSORPTION; AIR; PERCIFORM; PHOTORECEPTION; PREY CAPTURE; SPECIALIZATION; SPECTROPHOTOMETRY; VISION; WATER;

HEXAPODA; PISCES; TOXOTES CHATAREUS; VERTEBRATA;

EID: 77956940152     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.0345     Document Type: Conference Paper

References (84)

1. Allison, W. T., Haimberger, T. J., Hawryshyn, C. W. & Temple, S. E. 2004 Visual pigment composition in zebra-fish: evidence for a rhodopsin-porphyropsin interchange system. Vis. Neurosci. 21, 945-952.
2. Barta, A. & Horvath, G. 2003 Underwater binocular imaging of aerial objects versus the position of eyes relative to the flat water surface. J. Opt. Soc. Am. 20, 2370-2377. (doi:10.1364/JOSAA.20.002370)
3. Bekoff, M. & Dorr, R. 1976 Predation by 'shooting' in archer fish, Toxotes jaculatrix: accuracy and sequences. Bull. Psy-chonom. Soc. 7, 167-168.
4. Bowmaker, J. K. 1977 The visual pigments, oil droplets and spectral sensitivity of the pigeon. Vision Res. 17, 1129-1138. (doi:10.1016/0042-6989(77) 90147-X) (Pubitemid 8342708)
5. Bowmaker, J. K. 1991 The evolution of vertebrate visual pigments and photoreceptors. In Evolution of the eye and visual system, vol. 2 (eds J. R. Cronly-Dillon & R. L. Gregory), pp. 63-81. Boca Raton, FL: CRC Press, Inc.
6. Bowmaker, J. K., Govardovskii, V. I., Shukolyukov, S. A., Zueva, L. V., Hunt, D. M., Sideleva, V. G. & Smirnova, O. G. 1994 Visual pigments and the photic environment: the cottoid fish of Lake Baikal. Vision Res. 34, 591-605. (doi:10.1016/0042-6989(94)90015-9) (Pubitemid 24052164)
7. Bowmaker, J. K., Loew, E. R. & Ott, M. 2005 The cone photoreceptors and visual pigments of chameleons. J. Comp. Physiol. A 191, 925-932. (doi:10.1007/s00359-005-0014-4) (Pubitemid 41426193)
8. Braekevelt, C. R. 1985a Fine structure of the retinal pigment epithelial region of the archerfish (Toxotes jaculatrix). Ophthal. Res. 17, 221-229. (doi:10.1159/000265376)
9. Braekevelt, C. R. 1985b Photoreceptor fine structure in the archerfish (Toxotes jaculatrix). Am. J. Anat. 173, 89-98. (doi:10.1002/aja.1001730203) (Pubitemid 15037644)
10. Bridges, C. D. B. 1982 Porphyropsin in retina of four-eyed fish Anableps anableps. Nature 300, 384. (doi:10.1038/ 300384a0)
11. Britt, L. L., Loew, E. R. & McFarland, W. N. 2001 Visual pigments in the early life stages of Pacific northwest marine fishes. J. Exp. Biol. 204, 2581-2587.
12. Burkhardt, D. A., Gottesman, J., Levine, J. S. & MacNichol Jr, E. F. 1983 Cellular mechanisms for color-coding in holostean retinas and the evolution of color vision. Vision Res. 23, 1031-1041. (doi:10.1016/0042-6989(83)90014-7) (Pubitemid 14230416)
13. 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)
14. Carlisle, D. B. & Denton, E. J. 1959 On the metamorphosis of the visual pigments of Anguilla anguilla (L.). J. Mar. Biol. Assoc. UK 38, 97-102. (doi:10.1017/ S0025315400015629)
15. Collin, S. P. & Pettigrew, J. D. 1988 Retinal topography in reef teleosts 1: some species with well-developed areae but poorly-developed streaks. Brain Behav. Evol. 31, 269-282. (doi:10.1159/000116594)
16. Collin, S. P. & Pettigrew, J. D. 1989 Quantitative comparison of the limits on visual spatial resolution set by the ganglion cell layer in twelve species of reef teleosts. Brain Behav. Evol. 34, 184-192. (doi:10.1159/ 000116504)
17. Cummings, M. E. 2004 Modelling divergence in luminance and chromatic detection performance across measured divergence in surfperch (Embiotocidae) habitats. Vision Res. 44, 1127-1145. (doi:10.1016/j.visres.2003.12.013) (Pubitemid 38410816)
18. Cummings, M. E. & Partridge, J. C. 2001 Visual pigments and optical habitats of surfperch (Embiotocidae) in the California kelp forest. J. Comp. Physiol. A 187, 875-889.
19. Denton, E. J., Muntz, W. R. & Northmore, D. P. 1971 The distribution of visual pigment within the retina in two tele-osts. J. Mar. Biol. Assoc. UK 51, 905-915. (doi:10.1017/ S002531540001804X)
20. Dill, L. M. 1977 Refraction and the spitting behavior of archerfish (Toxotes chatareus). Behav. Ecol. Sociobiol. 2, 169-184.
21. Douglas, R. H. & Hawryshyn, C. W. 1990 Behavioural studies of fish vision: an analysis of visual capabilities. The visual system of fish. London, UK: Chapman & Hall.
22. Elshoud, G. C. A. & Koomen, P. 1985 A biomechanical analysis of spitting in archer fishes (Pisces, Perciformes, Toxidae). Zoomorphology 105, 240-252. (doi:10.1007/ BF00311967)
23. Ferree, C. E. & Rand, G. 1919 Chromatic thresholds of sensation from center to periphery of the retina and their bearing on color theory. Psychol. Rev. 26, 16-41. (doi:10.1037/h0071940)
24. Govardovskii, V. I., Fyhrquist, N., Reuter, T., Kuzmin, D. G. & Donner, K. 2000 In search of the visual pigment template. Vis. Neurosci. 17, 509-528. (doi:10.1017/ S0952523800174036)
25. Hart, N. S. 2002 Vision in the peafowl (Aves: Pavo cristatus). J. Exp. Biol. 205, 3925-3935.
26. Hart, N. S. 2004 Microspectrophotometry of visual pigments and oil droplets in a marine bird, the wedge-tailed shearwater Puffinus pacificus: topographic variations in photoreceptor spectral characteristics. J. Exp. Biol. 207, 1229-1240. (doi:10.1242/jeb.00857) (Pubitemid 38497885)
27. Hart, N. S. & Vorobyev, M. 2005 Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors. J. Comp. Physiol. A 191, 381-392. (doi:10.1007/s00359-004-0595-3) (Pubitemid 40534198)
28. Hart, N. S., Lisney, T. J. & Collin, S. P. 2006 Cone photo-receptor oil droplet pigmentation is affected by ambient light intensity. J. Exp. Biol. 209, 4776-4787. (doi:10. 1242/jeb.02568)
29. 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)
30. Helvik, J. V., Drivenes, O., Naess, T. H., Fjose, A. & Seo, H. C. 2001 Molecular cloning and characterization of five opsin genes from the marine flatfish Atlantic halibut (Hippoglossus hippoglossus). Vis. Neurosci. 18, 767-780.
31. Herald, E. S. 1956 How accurate is the archer fish? Pacific Discov. 9, 12-13.
32. Huang, Q. 1989 Intraretinal distribution of cone pigments in black porgy, Acanthopagrus schlegeli. Bull. Inst. Zool. Acad. Sin. 28, 175-182.
33. Kelber, A., Vorobyev, M. & Osorio, D. 2003 Animal colour vision-behavioural tests and physiological concepts. Biol. Rev. Camb. Phil. Soc. 78, 81-118.
34. Levine, J. S. & MacNichol, E. F. 1979 Visual pigments in tel-eost fishes: effects of habitat, microhabitat, and behavior on visual system evolution. Sens. Process. 3, 95-131.
35. Levine, J. S., MacNichol Jr, E. F., Kraft, T. & Collins, B. A. 1979 Intraretinal distribution of cone pigments in certain teleost fishes. Science 204, 523-526. (doi:10.1126/ science.432658)
36. Litherland, L. & Collin, S. P. 2008 Comparative visual function in elasmobranchs: spatial arrangement and ecological correlates of photoreceptor and ganglion cell distributions. Vis. Neurosci. 25, 549-561. (doi:10.1017/ S0952523808080693)
37. Loew, E. R. & Lythgoe, J. N. 1978 The ecology of cone pigments in teleost fish. Vision Res. 18, 715-722. (doi:10. 1016/0042-6989(78)90150-5)
38. Loew, E. R., McFarland, W. N. & Margulies, D. 2002 Developmental changes in the visual pigments of the yellowfin tuna, Thunnus albacares. Mar. Freshw. Behav. Physiol. 35, 235-246. (doi:10.1080/ 1023624021000003826)
39. L̈üling, K. H. 1956 Uber das Leuchtvermögen juveniler Tox-otes jaculatrix (Pallas 1766). Zool. Beiträge Bonn 7, 58.
40. Lüling, K. H. 1958 Morphologisch-anatomische und histo-logische Untersuchungen am Auge des Schützenfisches Toxotes jaculatrix (Pallas 1766) (Toxotidae), nebst Bemer-kungen zum Spuckgehaben. Zeitschrift für Morphologie und Ökologie der Tiere 47, 529-610. (doi:10.1007/BF00389870)
41. Lyall, A. H. 1957 Cone arrangements in teleost retinae. Q. J. Microsc. Sci. 98, 189.
42. Lythgoe, J. N. 1966 Visual pigments and underwater vision. In Light as an ecological factor, vol. 6 (eds R. Bainbidge, C. C. Evans & D. Rackham), pp. 375-391. Oxford, UK: Blackwell.
43. Lythgoe, J. N. & Partridge, J. C. 1989 Visual pigments and the acquisition of visual information. J. Exp. Biol. 146, 1-20.
44. Lythgoe, J. N., Muntz, W. R. A., Partridge, J. C., Shand, J. & Williams, D. M. 1994 The ecology of the visual pigments of snappers (Lutjanidae) on the Great Barrier Reef. J. Comp. Physiol. A 174, 461-467.
45. McDonald, C. G. & Hawryshyn, C. W. 1995 Intraspecific variation of spectral sensitivity in threespine stickleback (Gasterostreus aculeatus) from different photic regimes. J. Comp. Physiol. A 176, 255-260.
46. McFarland, W. N. & Munz, F. W. 1975 Part III. The evolution of photopic visual pigments in fishes. Vision Res. 15, 1071-1080 (doi:10.1016/0042-6989(75)90003-6)
47. Milburn, O., Alexander, R. & McN 1976 The performance of the muscles involved in spitting by the archefish Toxotes. J. Zool. 180, 243-251. (doi:10.1111/j.1469-7998.1976. tb04676.x)
48. Mullen, K. T. & Kingdom, F. A. A. 2002 Differential distributions of red-green and blue-yellow cone opponency across the visual field. Vis. Neurosci. 19, 109-118.
49. Myers, G. S. 1952 How the shooting apparatus of the archer fish was discovered. Aquarium J. 23, 210-214.
50. Neumeyer, C. 2003 Color vision in fishes and its neural basis. In Sensory processing in aquatic environments (eds S. P. Collin & N. J. Marshall), pp. 223-235. New York, NY: Springer.
51. Northmore, D. P. M., Oh, D. J. & Celenza, M. A. 2007 Acuity and contrast sensitivity of the bluegill sunfish and how they change during optic nerve regeneration. Vis. Neurosci. 24, 319-331.
52. Oliveira, F. G. et al. 2006 Topographic analysis of the ganglion cell layer in the retina of the four-eyed fish Ana-bleps anableps. Vis. Neurosci. 23, 879-886. (doi:10.1017/ S0952523806230232) (Pubitemid 46456694)
53. Osorio, D. & Vorobyev, M. 1996 Colour vision as an adaptation to frugivory in primates. Proc. R. Soc. Lond. B 263, 593-599. (doi:10.1098/rspb. 1996.0089) (Pubitemid 26169442)
54. Osorio, D. & Vorobyev, M. 2005 Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proc. R. Soc. Lond. B 272, 1745-1752. (doi:10.1098/rspb.2005.3156) (Pubitemid 41414652)
55. Owens, G. L., Windsor, D. J., Mui, J. & Taylor, J. S. 2009 A fish eye out of water: ten visual opsins in the four-eyed fish, Anableps anableps. PLoS One 4, e5970. (doi:10. 1371/journal.pone.0005970)
56. Panorgias, A., Parry, N. R. A., McKeefry, D. J., Kulikowski, J. J. & Murray, I. J. 2009 Nasal-temporal differences in cone-opponency in the near peripheral retina. Ophthal. Physiol. Opt. 29, 375-381. (doi:10.1111/j.1475-1313. 2009.00666.x)
57. Pettigrew, J. D. & Manger, P. R. 2008 Retinal ganglion cell density of the black rhinoceros (Diceros bicornis): calculating visual resolution. Vis. Neurosci. 25, 215-220.
58. Pignatelli, V., Champ, C., Marshall, J. & Vorobyev, M. 2010 Double cones are used for colour vision discrimination in reef fish, Rhinecanthis aculeatus. Biol. Lett. 6, 537-539. (doi:10.1098/rsbl.2009.1010)
59. Plotkin, A., Paperno, E., Vasserman, G. & Segev, R. 2008 Magnetic tracking of eye motion in small, fast-moving animals. IEEE Trans. Magnet. 44, 4492-4495. (doi: 10.1109/Tmag.2008.2002187).
60. Reuter, T. 1972 Long-lived photoproducts in the retinae of the frog and the crucian-carp. In Biochemistry and physiology of visual pigments (ed. H. Langer), pp. 211-217. Bochum, West Germany: Springer.
61. Reuter, T. E., White, R. H. & Wald, G. 1971 Rhodopsin and porphyropsin fields in the adult bullfrog retina. J. Gen. Physiol. 58, 351-371. (doi:10.1085/jgp.58.4.351)
62. Röhlich, P., van Veen, T. & Szel, A. 1994 Two different visual pigments in one retinal cone cell. Neuron 13, 1159-1166. (doi:10.1016/0896- 6273(94)90053-1) (Pubitemid 24372133)
63. Schlosser, J. A. 1764 An account of a fish from Batavia called Jaculator: in a letter to Mr. Peter Collinson, F. R. S. from John Albert Schlosser, M. D. F. R. S. Phil. Trans. R. Soc. Lond. 54, 89-91. (doi:10.1098/rstl.1764.0016)
64. Schuster, S., Rossel, S., Schmidtmann, A., Jager, I. & Por-alla, J. 2004 Archer fish learn to compensate for complex optical distortions to determine the absolute size of their aerial prey. Curr. Biol. 14, 1565-1568. (doi:10.1016/j.cub.2004.08.050) (Pubitemid 39290054)
65. Schuster, S., Wohl, S., Griebsch, M. & Klostermeier, I. 2006 Animal cognition: how archer fish learn to down rapidly moving targets. Curr. Biol. 16, 378-383. (doi:10.1016/j. cub.2005.12.037)
66. Segev, R., Schneidman, E., Goodhouse, J. & Berry, M. J. 2007 Role of eye movements in the retinal code for a size discrimination task. J. Neurophysiol. 98, 1380-1391. (doi:10.1152/jn.00395.2007) (Pubitemid 47435889)
67. Shand, J. 1993 Changes in the spectral absorption of cone visual pigments during the settlement of the goatfish Upenus tragula: the loss of red sensitivity as a benthic existence begins. J. Comp. Physiol. A 173, 115-121.
68. Simon, K. D. & Mazlan, A. G. 2008 Length-weight and length-length relationships of archer and puffer fish species. The Open Fish Sci. J. 1, 19-22. (doi:10.2174/ 1874401X00801010019)
69. Simon, K. D., Mazlan, A. G., Cob, Z. C., Samat, A. & Arshad, A. 2008 Age determination of archer fishes (To x-otes jaculatrix and Toxotes chatareus) inhabiting Malaysian estuaries. J. Biol. Sci. 8, 1096-1099. (doi:10.3923/jbs. 2008.1096.1099)
70. Simon, K. D., Bakar, Y., Samat, A., Zaidi, C. C., Aziz, A. & Mazlan, A. G. 2009 Population growth, trophic level, and reproductive biology of two congeneric archer fishes (Toxotes chatareus, Hamilton 1822 and Toxotes jaculatrix, Pallas 1767) inhabiting Malaysian coastal waters. J. Zhejiang Univ.-Sci. B 10, 902-911. (doi:10.1631/jzus. B0920173)
71. Szel, A., Rohlich, P., Caffe, A. R., Juliusson, B., Aguirre, G. & Vanveen, T. 1992 Unique topographic separation of two spectral classes of cones in the mouse retina. J. Comp. Neurol. 325, 327-342. (doi:10.1002/cne.903250302)
72. Szel, A., Rohlich, P., Caffe, A. R. & vanVeen, T. 1996 Distribution of cone photoreceptors in the mammalian retina. Microsc. Res. Tech. 35, 445-462. (doi:10.1002/ (SICI)1097-0029(19961215)35:6,445:AID-JEMT4. 3.0.CO;2-H)
73. Takechi, M. & Kawamura, S. 2005 Temporal and spatial changes in the expression pattern of multiple red and green subtype opsin genes during zebrafish development. J. Exp. Biol. 208, 1337-1345. (doi:10.1242/jeb.01532) (Pubitemid 40564568)
74. Temple, S. E. 2007 Effect of salinity on the refractive index of water: considerations for archer fish aerial vision. J. Fish Biol. 70, 1626-1629.
75. 2-based visual pigment composition during the life history of coho salmon (Oncorhynchus kisutch). J. Comp. Physiol. A 192, 301-313. (doi:10.1007/s00359-005-0068-3) (Pubitemid 43260976)
76. Temple, S. E., Ramsden, S. D., Haimberger, T. J., Veldhoen, K. M., Veldhoen, N. J., Carter, N. L., Roth, W.-M. & Hawryshyn, C. W. 2008a Effects of exogenous thyroid hormones on visual pigment composition in coho salmon (Oncorhynchus kisutch). J. Exp. Biol. 211, 2134-2143. (doi:10.1242/jeb.009365)
77. Temple, S. E., Veldhoen, K. M., Haimberger, T. J., Phelan, J. T., Veldhoen, N. J. & Hawryshyn, C. W. 2008b Ontogen-etic changes in cone photoreceptor spectral absorption and opsin expression in coho salmon (Oncorhynchus kisutch). J. Exp. Biol. 211, 3879-3888. (doi:10.1242/jeb. 020289)
78. Timmermans, P. J. A. 2000 Prey catching in the archer fish: marksmanship, and endurance of squirting at an aerial target. Netherlands J. Zool. 50, 411-423.
79. Timmermans, P. J. A. 2001 Prey catching in the archer fish: angles and probability of hitting an aerial target. Behav. Process. 55, 93-105. (doi:10.1016/S0376-6357(01)00172-3) (Pubitemid 32722228)
80. Timmermans, P. J. A. & Souren, P. M. 2004 Prey catching in archer fish: the role of posture and morphology in aiming behavior. Physiol. Behav. 81, 101-110. (doi:10.1016/j. physbeh.2004.01.010)
81. Timmermans, P. J. A. & Vossen, J. M. 2000 Prey catching in the archer fish: does the fish use a learned correction for refraction? Behav. Process. 52, 21-34. (doi:10.1016/ S0376-6357(00)00107-8)
82. Wagner, H. 1990 Retinal structure of fishes. The visual system of fish. London, UK: Chapman & Hall.
83. Wood, P., Partridge, J. C. & Grip, W. 1992 Rod visual pigment changes in the elver of the eel Anguilla anguilla L. measured by microspectrophotometry. J. Fish Biol. 41, 601-611. (doi:10.1111/j.1095-8649. 1992.tb02686.x)
84. Yoshizawa, T. 1994 Molecular basis for color vision. Biophys. Chem. 50, 17-24. (doi:10.1016/0301-4622(94)85016-X)