Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-24T13:26:32.409Z Has data issue: false hasContentIssue false
  • English
  • Français

Spectral sensitivities of the seahorses Hippocampus subelongatus and Hippocampus barbouri and the pipefish Stigmatopora argus

Published online by Cambridge University Press:  06 September 2007

VIRGINIA MOSK ,
NICOLE THOMAS ,
NATHAN S. HART ,
JULIAN C. PARTRIDGE ,
LYN D. BEAZLEY  and
JULIA SHAND
VIRGINIA MOSK
Affiliation:
School of Animal Biology, University of Western Australia, Western Australia
NICOLE THOMAS
Affiliation:
School of Animal Biology, University of Western Australia, Western Australia
NATHAN S. HART
Affiliation:
Vision, Touch & Hearing Research Centre, University of Queensland, Queensland, Australia
JULIAN C. PARTRIDGE
Affiliation:
School of Biological Sciences, University of Bristol, Bristol, United Kingdom
LYN D. BEAZLEY
Affiliation:
School of Animal Biology, University of Western Australia, Western Australia
JULIA SHAND
Affiliation:
School of Animal Biology, University of Western Australia, Western Australia
Get access Rights & Permissions [Opens in a new window]

Abstract

The Syngnathidae are specialized diurnal feeders that are known to possess a retinal fovea and use independent eye movements to locate, track, and strike individual planktonic prey items. In this study, we have investigated the spectral sensitivities of three syngnathid species: a pipefish and two seahorses. We used spectrophotometry to measure the spectral transmission properties of ocular lenses and microspectrophotometry to measure the spectral absorption characteristics of visual pigments in the retinal photoreceptors. The pipefish, Stigmatopora argus, together with the seahorse Hippocampus subelongatus, is found in “green-water” temperate coastal seagrass habitats, whereas the second seahorse, H. barbouri, originates from a “blue-water” tropical coral reef habitat. All species were found to possess short wavelength absorbing pigment(s) in their lenses, with the 50% cut-off point of S. argus and H. subelongatus at 429 and 425 nm respectively, whereas that of H. barbouri was located at 409 nm. Microspectrophotometry of the photoreceptors revealed that the rods of all three species contained visual pigment with the wavelength of maximum absorption (λmax) at approximately 500 nm. The visual pigment complement of the cones varied between the species: all possessed single cones with a λmax close to 460 nm but H. barbouri also possessed an additional class of single cone with λmax at 430 nm. Three classes of visual pigment were found in the double cones, the λmax being approximately 520, 537, and 560 nm in the two seahorses and 520, 537, and 580 nm in the pipefish. The spectral sensitivities of the syngnathids investigated here do not appear to conform to generally accepted trends for fishes inhabiting different spectral environments. The influence of the specialized feeding regime of the syngnathids is discussed in relation to our findings that ultra-violet sensitivity is apparently not necessary for zooplanktivory in certain habitats.

Keywords

Ocular lensesVisual pigmentsPhotoreceptorsMicrospectrophotometrySyngnathidae
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 3 , May 2007 , pp. 345 - 354
Copyright
© 2007 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bayliss, L.E., Lythgoe, R.J. & Tansley, K. (1936). Some new forms of visual purple found in sea fishes with a note on the visual cells of origin. Proceedings of the Royal Society B 120, 95–113.CrossRefGoogle Scholar
Bennet, B.A. & Branch, G.M. (1990). Relationships between production and consumption of prey species by resident fish in the Bot, a cool temperate South African estuary. Estuarine, Coastal and Shelf Science 31, 139–155.CrossRefGoogle Scholar
Bergert, B.A. & Wainwright, P.C. (1997). Morphology and kinematics of prey capture in the syngnathid fishes Hippocampus erectus and Syngnathus floridae. Marine Biology 127, 563–570.CrossRefGoogle Scholar
Blatz, P.E. & Liebman, P.A. (1973). Wavelength regulation in visual pigments. Experimental Eye Research 17, 573–580.CrossRefGoogle Scholar
Bowmaker, J.K. (1995). The visual pigments of fish. Progress in Retinal & Eye Research 15, 1–31.CrossRefGoogle Scholar
Bowmaker, J.K., Govardovskii, V.I., Zueva, L.V., Hunt, D.M. & Sideleva, V. (1994). Visual pigments and the photic environment: The Cottoid fish of Lake Baikal. Vision Research 34, 591–605.CrossRefGoogle Scholar
Bowmaker, J.K. & Hunt, D.M. (2006). Evolution of vertebrate visual pigments. Current Biology 16, 484–489.CrossRefGoogle Scholar
Bowmaker, J.K. & Kunz, Y.W. (1987). Ultraviolet receptors, tetrachromatic colour vision and retinal mosaics in the brown trout (Salmo trutta): Age dependent change. Vision Research 27, 2101–2108.CrossRefGoogle Scholar
Britt, L.L., Loew, E.R. & McFarland, W.N. (2001). Visual pigments in the early life history stages of Pacific northwest marine fishes. Journal of Experimental Biology 204, 2581–2587.Google Scholar
Browman, H.I., Novales Flamarique, I. & Hawryshyn, C.W. (1994). Ultraviolet photoreception contributes to the foraging performance of two species of zooplanktivorous fishes. Journal of Experimental Biology 186, 187–198.Google Scholar
Campolmi, M., Franzoi, P. & Mazzola, A. (1996). Observations on pipefish (Syngnathidae) biology in the Stagnone lagoon (west Sicily). Publicaciones Especiales Instituto Español de Oceanografía 21, 205–209.Google Scholar
Clarke, G.L. (1936). On the depth at which fishes can see. Ecology 17, 452–456.CrossRefGoogle Scholar
Collin, S.P. & Collin, H.B. (1999). The foveal photoreceptor mosaic in the pipefish, Corythoichthyes paxtoni (Syngnathidae, Teleostei). Histology & Histopathology 14, 369–382.Google Scholar
Collin, S.P. & Shand, J. (2003). Retinal sampling and the visual field in fishes. In Sensory Processing of the Aquatic Environment, ed. Collin, S.P. & Marshall, N.J., pp. 139–169. New York: Springer Verlag.CrossRef
Cummings, M.E. & Partridge, J.C. (2001). Visual pigments and optical habitats of surfperch (Embiotocidae) in the Californian kelp forest. Journal of Comparative Physiology A 187, 875–889.Google Scholar
Denton, E.J. & Warren, F.J. (1957). The photosensitive pigments in the retinae of deep-sea fish. Journal of the Marine Biological Association UK 36, 651–662.CrossRefGoogle Scholar
Deutschlander, M.E., Greaves, D.K., Haimberger, T.J. & Hawryshyn, C.W. (2001). Functional mapping of ultraviolet photosensitivity during metamorphic transitions in a salmonid fish, Onchorhynchus mykiss. Journal of Experimental Biology 204, 2401–2413.Google Scholar
Douglas, R.H. (2001). The ecology of teleost fish visual pigments a good example of sensory adaptation to the environment? In Ecology of Sensing, ed. Schmid, A., pp. 215–235. Berlin: Springer-Verlag.
Douglas, R.H., Hunt, D.M. & Bowmaker, J.K. (2003). Spectral sensitivity tunning in the deep-sea. In Sensory Processing of the Aquatic Environment, ed. Collin, S.P. & Marshall, N.J., pp. 323–342. New York: Springer Verlag.CrossRef
Flynn, A.J. & Ritz, D.A. (1999). Effect of habitat complexity and predatory style on the capture success of fish feeding on aggregated prey. Journal of the Marine Biological Association UK 79, 487–494.CrossRefGoogle Scholar
Fritches, K.A., Litherland, L., Thomas, N. & Shand, J. (2003). Cone visual pigments and retinal mosaics in the striped marlin. Journal of Fish Biology 63, 1347–1351.CrossRefGoogle Scholar
Fuller, R.C., Carleton, K.L., Fadool, J.M., Spady, T.C. & Travis, J. (2004). Population variation in opsin expression in the bluefin killifish, Lucania goodie. Journal of Comparative Physiology A 190, 147–154.CrossRefGoogle Scholar
Govardovskii, V.I., Fyhrquist, N., Reuter, T., Kuzman, D.G. & Donner, K. (2000). In search of the visual pigment template. Visual Neuroscience 17, 509–528.CrossRefGoogle Scholar
Hart, N.S., Partridge, J.C., Bennett, A.T.D. & Cuthill, I.C. (2000). Visual pigments, cone oil droplets and ocular media in four species of estrildid finch. Journal of Comparative Physiology A 186, 681–694.CrossRefGoogle Scholar
Hawryshyn, C.W., Arnold, M.G., Chiasson, D.J. & Martin, P.C. (1989). The ontogeny of ultraviolet photosensitivity in rainbow trout (Salmo gairdneri). Visual Neuroscience 2, 247–254.CrossRefGoogle Scholar
Hochberg, E.J., Atkinson, M.J., Apprill, A. & Adréfouët, S. (2004). Spectral reflectance of coral. Coral Reefs 23, 84–95.CrossRefGoogle Scholar
Hoffman, M., Tripathi, N., Henz, S.R., Lindholm, A.K., Weigel, D., Breden, F. & Dreyer, C. (2007). Opsin gene duplication and diversification in the guppy, a model for sexual selection. Proceedings of the Royal Society of London B 274, 33–42.CrossRefGoogle Scholar
Howard, R.K. & Koehn, J.D. (1985). Population dynamics and feeding ecology of pipefish (Syngnathidae) associated with eelgrass beds of Western Port, Victoria, Australia. Australian Journal of Marine & Freshwater Research 36, 361–370.CrossRefGoogle Scholar
Hunt, D.M., Wilkie, S.E., Bowmaker, J.K. & Poopalasundaram, S. (2001). Vision in the ultraviolet. Cellular and Molecular Life Sciences 58, 1583–1598.CrossRefGoogle Scholar
James, P.L. & Heck, K.L. (1994). The effects of habitat complexity and light intensity on ambush predation within a simulated seagrass habitat. Journal of Experimental Marine Biology & Ecology 176, 187–200.CrossRefGoogle Scholar
Kendrick, A.J. (2002). Resource utilisation and reproductive biology of syngnathid fishes in a seagrass-dominated marine environment in south-western Australia. PhD Thesis. Murdoch University, Western Australia.
Krauss, A. & Neumeyer, C. (2003). Wavelength dependence of the optomotor response in zebrafish (Danio rerio). Vision Research 43, 1273–1282.CrossRefGoogle Scholar
Kroger, R.H.H., Knoblauch, B. & Wagner, H.J. (2003). Rearing in different photic and spectral environments changes the optomotor response to chromatic stimuli in the cichlid fish Aequidens pulcher. Journal of Experimental Biology 206, 1643–1648.CrossRefGoogle Scholar
Kuiter, R. (2000). Seahorses, pipefish and their relatives. A comprehensive guide to Syngnathiformes. Chorleywood, England: TMC Publishing.
Levine, J.S. & MacNichol, E.F.J. (1979). Visual pigments in teleost fishes: Effects of habitat, microhabitat, and behaviour on visual system evolution. Sensory Processes 3, 95–131.Google Scholar
Levine, J.S. & MacNichol, E.F.J. (1985). Microspectrophotometry of primate photoreceptors: Art, artefact, and analysis. In The Visual System, ed. Fein, A. & Levine, J.S., pp. 73–87. New York: Liss.
Loew, E.R. & Lythgoe, J.N. (1978). The ecology of cone pigments in teleost fishes. Vision Research 18, 715–722.CrossRefGoogle Scholar
Loew, E.R., McFarland, W.N., Mills, E.L. & Hunter, D. (1993). A chromatic action spectrum for planktonic predation by juvenile yellow perch, Perca flavescens. Canadian Journal of Zoology 71, 384–386.CrossRefGoogle Scholar
Losey, G.S., Cronin, T.W., Goldsmith, T.H., Hydes, D., Marshall, N.J. & McFarland, W.N. (1999). The UV visual world of fishes: A review. Journal of Fish Biology 54, 921–943.CrossRefGoogle Scholar
Losey, G.S., McFarland, W.N., Loew, E.R., Zamzow, J.P., Nelson, P.A. & Marshall, N.J. (2003). Visual biology of Hawaiian coral reef fishes. I. Ocular transmission and visual pigments. Copeia 2003, 433–454.Google Scholar
Lourie, S.A., Vincent, A.C.J. & Hall, H.J. (1999). Seahorses. An identification guide to the world's species and their conservation. London, England: Project Seahorse.
Lourie, S.A. & Randall, J.E. (2003). A new pygmy seahorse: Hippocampus denise (Teleostei: Syngnathidae) from the Indopacific. Zoological Studies 42, 284–291.Google Scholar
Lythgoe, J.N. (1984). Visual pigments and environmental light. Vision Research 24, 1539–1550.CrossRefGoogle Scholar
Lythgoe, J.N. (1979). The Ecology of Vision. Oxford, England: Clarendon Press.
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. Journal of Comparative Physiology A 174, 461–467.Google Scholar
Lythgoe, J.N. & Partridge, J.C. (1989). Visual pigments and the acquisition of visual information. Journal of Experimental Biology 146, 1–20.Google Scholar
Lythgoe, J.N. & Partridge, J.C. (1991). The modelling of optimal visual pigments of dichromatic teleosts in green coastal waters. Vision Research 31, 361–371.CrossRefGoogle Scholar
MacNichol, E.F. (1986). A unifying presentation of photopigment spectra. Vision Research 26, 1543–1556.CrossRefGoogle Scholar
Marshall, N.J. & Vorobyev, M. (2003). The design of color signals and color vision in fishes. In Sensory Processing of the Aquatic Environment, ed. Collin, S.P. & Marshall, N.J., pp. 194–222. New York: Springer-Verlag.CrossRef
Marshall, N.J., Jennings, K., McFarland, W.N., Loew, E.R. & Losey, G.S. (2003). Visual biology of Hawaiian coral reef fishes. III. Environmental light and an integrated approach to the ecology of reef fish vision. Copeia 203, 455–466.Google Scholar
Marshall, N.J., Vorobyev, M. & Siebeck, U.E. (2006). What does a reef fish see when it sees a reef fish? Eating “Nemo.” In Communication in Fishes, ed. Ladich, F., Collin, S.P., Moller, P. & Kapoor, B.G., pp. 393–422. Enfield: Science Publishers.
Matsumoto, Y., Fukamach, S., Mitam, H. & Kawamura, S. (2006). Functional characterisation of visual opsin repertoire in Medaka (Oryzias latipes). Gene 371, 268–278.Google Scholar
McFarland, W.N. & Loew, E.R. (1994). Ultraviolet visual pigments in marine fishes of the family pomacentridae. Vision Research 34, 1393–1396.CrossRefGoogle Scholar
Mosk, V.J. (2004). The visual system of seahorses and pipefish: A study of visual pigments and other characteristics. MSc. Thesis, University of Western Australia.
Munz, F.W. (1958). Photosensitive pigments from the retinae of certain deep-sea fishes. Journal of Physiology 140, 1575–1580.Google Scholar
Neumeyer, C. (1986). Wavelength discrimination in the goldfish. Journal of Comparative Physiology A 158, 203–213.CrossRefGoogle Scholar
Neumeyer, C. (1992). Tetrachromatic color vision in goldfish: Evidence from color mixture experiments. Journal of Comparative Physiology A 171, 639–649.CrossRefGoogle Scholar
Parry, J.W.L., Carleton, K.L., Spady, T., Carboo, A., Hunt, D.M. & Bowmaker, J.K. (2005). Mix and match colour vision: Tuning spectral sensitivity by differential opsin gene expression in Lake Malawi cichlids. Current Biology 15, 1734–1739.CrossRefGoogle Scholar
Partridge, J.C. (1990). The colour sensitivity and vision of fishes. In Light and Life in the Sea, ed. Herring, P.J., Campbell, A.K. & Whitfield, M., pp. 167–184. Cambridge, England: Cambridge University Press.
Partridge, J.C. & Cummings, M.E. (1999). Adaptation of visual pigments to the aquatic environment. In Adaptive Mechanisms in the Ecology of Vision, ed. Archer, S.N., Djamgoz, M.B.A., Loew, E.R., Partridge, J.C. & Vallerga, S., pp. 251–284. Dordrechet, Holland: Kluwer.CrossRef
Partridge, J.C., Speare, P., Shand, J., Muntz, W.R.A. & Williams, D.M. (1992). Microspectrophotometric determinations of rod visual pigments in some adult and larval Australian amphibians. Visual Neuroscience 9, 137–142.CrossRefGoogle Scholar
Paulus, T. (1994a). Morphology of the head skull and the tube snout of the Syngnathidae from the Red Sea (Pieces: Teleostei). Senckenbergiana Maritima 21, 53–62.Google Scholar
Paulus, T. (1994b). Calculation of the niche breadth and niche overlapping based on digestive system content analysis of three synoptic Syngnathidae from the Red Sea. Senckenbergiana Maritima 25, 63–74.Google Scholar
Reckel, F., Melzer, R.R., Parry, J.W.L. & Bowmaker, J.K. (2002). The retina of five atherinomorph teleosts: Photoreceptors, patterns and spectral sensitivities. Brain Behavior and Evolution 60, 249–264.CrossRefGoogle Scholar
Ryer, C.H. & Orth, R.J. (1987). Feeding ecology of the Northern pipefish, Syngnathus fuscus, in a seagrass community of the lower Chesapeake Bay. Estuaries 10, 330–336.CrossRefGoogle Scholar
Salih, A., Larkum, A., Cox, G., Kuhl, M. & Hoegh-Guldberg, O. (2000). Flourescent pigments in coral are photoprotective. Nature 408, 850–853.CrossRefGoogle Scholar
Schaerer, S. & Neumeyer, C. (1996). Motion detection in goldfish investigated with the optomotor response is “color blind.” Vision Research 36, 4025–4034.Google Scholar
Shand, J. (1993). Changes in the absorption spectrum of cone visual pigments during settlement of the goatfish Upeneus tragula: loss of red sensitivity as a benthic existence begins. Journal of Comparative Physiology A 173, 115–121.Google Scholar
Shand, J., Hart, N.S., Thomas, N. & Partridge, J.C. (2002). Developmental changes in the visual pigments of back bream, Acanthopagrus butcheri. Journal of Experimental Biology 205, 3661–3667.Google Scholar
Sheng, J.Q., Lin, Q., Chen, Q.X., Gao, Y., Shen, L. & Lu, J.Y. (2006). Effects of food, temperature and light intensity on the feeding behavior of three-spot juvenile seahorses, Hippocampus trimaculatus Leach. Aquaculture 1–4, 596–607.CrossRefGoogle Scholar
Shibata, K. (1969). Pigments and a UV-absorbing substance in corals and a blue-green alga living in the Great Barrier Reef. Plant and Cell Physiology 10, 325–335.Google Scholar
Siebeck, U.E. & Marshall, N.J. (2001). Ocular media transmission of coral reef fish—can coral reef fish see ultraviolet light? Vision Research 41, 133–149.Google Scholar
Spady, T.C., Parry, J.W.L., Robinson, P.R., Hunt, D.M., Bowmaker, J.K. & Carleton, K.L. (2006). Evolution of the cichlid visual palette through ontogenetic subfunctionalization of the opsin gene arrays. Molecular Biology and Evolution 23, 1538–1547.CrossRefGoogle Scholar
Steffe, A.S., Westoby, M. & Bell, J.D. (1989). Habitat selection and diet in two species of pipefish from seagrass: Sex differences. Marine Ecology Progress Series 55, 23–30.CrossRefGoogle Scholar
Teixeira, R.L. & Musick, J.A. (2001). Reproduction and food habits of the lined seahorse, Hippocampus erectus (Teleostei: Syngnathidae) of Chesapeake Bay, Virginia. Brazilian Journal of Biology 61, 79–90.Google Scholar
Thorpe, A., Douglas, R.H. & Truscott, R.J.W. (1993). Spectral transmission of short-wave absorbing pigments in the fish lens—I. Phylogenetic distribution and identity. Vision Research 33, 289–300.Google Scholar
Ute-Palm, A.C. & Bowmaker, J.K. (2006). Spectral sensitivity of the two-spotted goby Gobiusculus flavescens (Fabricus): A physiological and behavioural study. Journal of Experimental Biology 209, 2034–2041.CrossRefGoogle Scholar
Vincent, A.C.J. & Sadler, L.M. (1995). Faithful pair bonds in wild seahorses: Hippocampus whitei. Animal Behaviour 50, 1557–1569.CrossRefGoogle Scholar
Walls, G.L. (1942). The Vertebrate Eye and its Adaptive Radiation. Michigan: Cranbrook Institute of Science.CrossRef