Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-23T17:07:46.516Z Has data issue: false hasContentIssue false
  • English
  • Français

The morphology of the dorsal eye of the hydrothermal vent shrimp, Rimicaris exoculata

Published online by Cambridge University Press:  02 June 2009

Patrick J. O'Neill ,
Robert N. Jinks ,
Erik D. Herzog ,
Barbara-Anne Battelle ,
Leonard Kass ,
George H. Renninger  and
Steven C. Chamberlain
Patrick J. O'Neill
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse
Robert N. Jinks
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse Institute for Sensory Research, Syracuse University, Syracuse
Erik D. Herzog
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse Institute for Sensory Research, Syracuse University, Syracuse
Barbara-Anne Battelle
Affiliation:
The Whitney Laboratory, University of Florida, St. Augustine
Leonard Kass
Affiliation:
Department of Zoology, University of Maine, Orono
George H. Renninger
Affiliation:
Biophysics Group, Department of Physics, University of Guelph, Guelph
Steven C. Chamberlain
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse Institute for Sensory Research, Syracuse University, Syracuse
Get access Rights & Permissions [Opens in a new window]

Abstract

The bresiliid shrimp, Rimicaris exoculata, lives in large masses on the sides of hydrothermal vent chimneys at two sites on the Mid-Atlantic Ridge. Although essentially no daylight penetrates to depths of 3500 m, very dim light is emitted from the hydrothermal vents themselves. To exploit this light, R. exoculata has evolved a modified compound eye on its dorsal surface that occupies about 0.5% of the animal's body volume. The eye's morphology suggests that it is extremely sensitive to light. The cornea of the dorsal eye is smooth with no dioptric apparatus. The retina consists of two wing-shaped lobes that are fused across the midline anteriorly. The rhabdomeral segments of the 7000 ommatidia form a compact layer of photosensitive membrane with an entrance aperture of more than 26 mm2. Within this layer, the volume density of rhabdom is more than 70%. Below the rhabdomeral segments, a thick layer of white diffusing cells scatters light upward into the photoreceptors. The arhabdomeral segments of the five to seven photoreceptors of each ommatidium are mere strands of cytoplasm that expand to accommodate the photoreceptor nuclei. The rhabdom is comprised of well-organized arrays of microvilli, each with a cytoskeletal core. The rhabdomeral segment cytoplasm contains mitochondria, but little else. The perikaryon contains a band of mitochondria, but has only small amounts of endoplasmic reticulum. There is no ultrastructural indication of photosensitive membrane cycling in these photoreceptors. Vestigial screening pigment cells and screening pigment granules within the photoreceptors are both restricted to the inner surface of the layer of the white diffusing cells. Below the retina, photoreceptor axons converge in a fan-shaped array to enter the dorsal surface of the brain. The eye's size and structure are consistent with a role for vision in shrimp living at abyssal hydrothermal vents.

Keywords

Bresiliid shrimpInvertebrate photoreceptorsDeep sea visionMid-Atlantic RidgeDSV Alvin
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 5 , September 1995 , pp. 861 - 875
Copyright
Copyright © Cambridge University Press 1995

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

Chamberlain, S.C. & Hornstein, E.P. (1993). Photoreceptors, black smokers, and seasonal affective disorder: Evidence for photosta-sis. In Sensory Research, Multimodal Perspectives, ed. Verrillo, R.T., pp. 105–118. Hillsdale, New Jersey: Lawrence Erlbaum Associates, Publishers.Google Scholar
Chamberlain, S.C., Lakin, R.C., Wharton, D.N., Nuckley, D.J., Kuenzler, R.O., Kwasniewski, J.T., O'Neill, P.J., Jinks, R.N., Herzog, E.D. & Verrillo, R.T. (1994a). Retinal structure in hydro-thermal vent shrimp from the Mid-Atlantic Ridge. Society for Neuroscience Abstracts 20, 132.Google Scholar
Chamberlain, S.C., Lakin, R.C., Wharton, D.N., Nuckley, D.J., Kuenzler, R.O., Kwasniewski, J.T., O'Neill, P.J., Jinks, R.N. & Herzog, E.D. (1994b). Vision in hydrothermal vent shrimp: Unusual structures for seeing in an unusual environment. Annals of Biomedical Engineering (Suppl. 1) 22, 56.Google Scholar
Chamberlain, S.C., Meyer-Rochow, V.B. & Dossert, W.P. (1986). Morphology of the compound eye of the giant deep-sea isopod Bathynomus giganteus. Journal of Morphology 189, 145–156.CrossRefGoogle ScholarPubMed
Clarke, G.L. & Denton, E.J. (1962). Light and animal life. In The Sea, ed. Hill, M.N., pp. 456–468. London, England: Interscience.Google Scholar
Clarke, G.L. & Kelly, M.G. (1964). Variation in transparency and in bioluminescence on longitudinal transects in the western Indian Ocean. Bulletin of the Institute for Oceanography, Monaco 64, 1–20.Google Scholar
Corliss, J.B., Dymond, J., Gordon, L.I., Edmond, J.M., von Her-zen, R.P., Ballard, R.D., Green, K., Williams, D., Bainbridge, A., Crane, K. & van Andel, T.H. (1979). Submarine thermal springs on the Galápagos Rift. Science 203, 1073–1083.CrossRefGoogle ScholarPubMed
Doughtie, D.G. & Rao, K.R. (1984). Ultrastructure of the eye of the grass shrimp, Palaemonetes pugio. General morphology, and light and dark adaptation at noon. Cell and Tissue Research 238, 271–288.CrossRefGoogle Scholar
Elofsson, R. & Hallberg, E. (1977). Compound eyes of some deep-sea and fiord mysid crustaceans. Acta Zoologica (Stockholm) 58, 169–177.CrossRefGoogle Scholar
Foxton, P. (1970). The vertical distribution of pelagic decapods (Crustacea: Natantia) collected on the SOND Cruise (1965). I. The Caridea. Journal of the Marine Biological Association of the United Kingdom 50, 939–960.CrossRefGoogle Scholar
Grassle, J.F. (1985). Hydrothermal vent animals: Distribution and biology. Science 229, 713–717.CrossRefGoogle ScholarPubMed
Hornstein, E.P. & Chamberlain, S.C. (1991). Correlation of photoreceptor structure and lighting environment: Implications for photo-stasis. Society for Neuroscience Abstracts 17, 298.Google Scholar
Hose, J.E., Martin, G.G. & Gerard, A.S. (1990). A decapod hemo-cyte classification scheme integrating morphology, cytochemistry, and function. Biological Bulletin 178, 33–45.CrossRefGoogle ScholarPubMed
Itaya, S.K. (1976). Rhabdom changes in the shrimp, Palaemonetes. Cell and Tissue Research 166, 265–273.CrossRefGoogle ScholarPubMed
Kampa, E.M. (1970). Underwater daylight and moonlight measurements in the eastern North Atlantic. Journal of the Marine Biological Association of the United Kingdom 50, 391–420.CrossRefGoogle Scholar
Loew, E. (1976). Light, and photoreceptor degeneration in the Norway lobster, Nephrops norvegicus (L.). Proceedings of the Royal Society B (London) 193, 31–44.Google ScholarPubMed
Lythgoe, J.N. (1979). The Ecology of Vision. Oxford: Clarendon Press, 244 p.Google Scholar
Nilsson, H.L. & Lindström, M. (1983). Retinal damage and sensitivity loss of a light-sensitive crustacean compound eye (Cirolana borealis): Electron microscopy and electrophysiology. Journal of Experimental Biology 107, 277–292.CrossRefGoogle Scholar
O'Neill, P.J., Jinks, R.N., Herzog, E.D. & Chamberlain, S.C. (1994). Is photoreceptor membrane shedding ubiquitous? Negative evidence from an ultra-high sensitivity photoreceptor. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1520.Google Scholar
Pelli, D.G. & Chamberlain, S.C. (1989). The visibility of 350°C black-body radiation by the shrimp Rimicaris exoculata and man. Nature 337, 460–461.CrossRefGoogle Scholar
Rona, P.A. (1985). Black smokers and massive sulfides at the TAG Hydrothermal Field, Mid-Atlantic Ridge 26°N. Eos, Transactions, American Geophysical Union 66, 936.CrossRefGoogle Scholar
Rona, P.A. (1992). Deep-sea geysers of the Atlantic. National Geographic 182, 104–109.Google Scholar
Rona, P.A., Klinkhammer, G., Nelsen, T.A., Trefry, J.H. & Elder-field, H. (1986). Black smokers, massive sulfides and vent biota at the Mid-Atlantic Ridge. Nature 321, 33–37.CrossRefGoogle Scholar
Segonzac, M., de Saint Laurent, M. & Casanova, B. (1994). L'énigme du comportement trophique des crevettes Alvinocaridi-dae des sites hydrothermaux de la dorsale médio-atlantique. Cahiers de Biologie Marine 34, 535–571.Google Scholar
Shelton, P.M.J., Gaten, E. & Chapman, C.J. (1985). Light and retinal damage in Nephrops norvegicus (L.). Proceedings of the Royal Society B (London) 226, 217–236.Google Scholar
Tsukita, S., Tsukita, S. & Matsumoto, G. (1988). Light-induced structural changes of cytoskeleton in squid photoreceptor microvilli detected by rapid-freeze method. Journal of Cell Biology 106, 1151–1160.CrossRefGoogle ScholarPubMed
Tunnicliffe, V. (1992). Hydrothermal-vent communities of the deep sea. American Scientist 80, 336–349.Google Scholar
Van Dover, C.L., Szuts, E.Z., Chamberlain, S.C. & Cann, J.R. (1989). A novel eye in ‘eyeless’ shrimp from hydrothermal vents of the Mid-Atlantic Ridge. Nature 337, 458–460.CrossRefGoogle ScholarPubMed
Van Dover, C.L., Cann, J.R., Cavanaugh, C., Chamberlain, S., Delaney, J.R., Janecky, D., Imhoff, J., Tyson, J.A. & the LITE Workshop participants (1994). Light at deep sea hydrothermal vents. Eos, Transactions, American Geophysical Union 75, 44–45.CrossRefGoogle Scholar
Williams, A.B. & Rona, P.A. (1986). Two new caridean shrimps (Bresiliidae) from a hydrothermal field on the Mid-Atlantic Ridge. Journal of Crustacean Biology 6, 446–462.CrossRefGoogle Scholar