Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-26T10:18:09.122Z Has data issue: false hasContentIssue false
  • English
  • Français

Retinal Anatomy of New Bresiliid Shrimp from the Lucky Strike and Broken Spur Hydrothermal Vent Fields on the Mid-Atlantic Ridge

Published online by Cambridge University Press:  11 May 2009

R.O. Kuenzler ,
J.T. Kwasniewski ,
R.N. Jinks ,
R.C. Lakin ,
B.A. Battelle ,
E.D. Herzog ,
L. Kass ,
G.H. Renninger  and
S.C. Chamberlin
R.O. Kuenzler
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse, New York 13244–1240, USA
J.T. Kwasniewski
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse, New York 13244–1240, USA
R.N. Jinks
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse, New York 13244–1240, USA Institute for Sensory Research, Syracuse University, Syracuse, New York, 13244–5290, USA
R.C. Lakin
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse, New York 13244–1240, USA
B.A. Battelle
Affiliation:
The Whitney Laboratory, University of Florida, St Augustine, Florida 32086, USA
E.D. Herzog
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse, New York 13244–1240, USA Institute for Sensory Research, Syracuse University, Syracuse, New York, 13244–5290, USA
L. Kass
Affiliation:
Department of Zoology, University of Maine, Orono, Maine 04469, USA
G.H. Renninger
Affiliation:
Biophysics Group, Department of Physics, University of Guelph, Guelph, Ontario, Canada, NIG 2W1
S.C. Chamberlin
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse, New York 13244–1240, USA
Get access Rights & Permissions [Opens in a new window]

Extract

The 1989 discovery of a large dorsal eye on the hydrothermal vent shrimp, Rimicaris exoculata, debunked the prevailing opinion that all animals living around deep hydrothermal vents were blind. Recent dives with DSV ‘Alvin’ recovered new bresiliid shrimp [Chorocaris (Lucky Strike) and Chorocaris (Broken Spur)] from two new vent fields on the Mid-Atlantic Ridge. The Lucky Strike species has recently been named Chorocaris fortunata and may be the same as the Broken Spur species - the retinal morphologies reported here are very similar. Like R. exoculata, C. fortunata has a visual apparatus adapted to the very dim light of its environment. Although in both species enlarged, non-imaging eyes appear to have evolved from the stalked compound eyes typical of caridean shrimp, those of C. fortunata are forward-facing whilst that of R. exoculata is located dorsally. The massive array of photosensitive membrane (rhabdom) of C. fortunata lies beneath a smooth cornea within a matt, white, reflecting matrix and occupies 80% of the available volume of the photoreceptors compared to the expected 10–15% of shallow water decapods. All screening pigment is located out of the light path at the bottom of the retina. There is no ultrastructural evidence for cyclic rhabdom shedding or renewal. Thus the cellular organization of C. fortunata is remarkably similar to that of R. exoculata and distinct from its surface-dwelling relatives. This suggests that in these species imaging optics have been sacrificed to achieve the increased visual sensitivity necessary to detect the very dim light emitted from the throats of the black smoker chimneys around which they live

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 77 , Issue 3 , August 1997 , pp. 707 - 725
Copyright
Copyright © Marine Biological Association of the United Kingdom 1997

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

Behrens, M. & Krebs, W., 1976. The effect of light-dark adaptation on the ultrastructure of Limulus lateral eye retinular cells. Journal of Comparative Physiology, 107, 77–96.CrossRefGoogle Scholar
Blest, A.D. & Day, W.A., 1978. The rhabdomere organization of some nocturnal pisaurid spiders in light and darkness. Philosophical Transactions of the Royal Society B, 283, 1–23.Google Scholar
Chamberlain, S.C. & Hornstein, E.P., 1993. Photoreceptors, black smokers, and seasonal affective disorder: evidence for photostasis. In Sensory research, multimodal perspectives (ed. R.T, Verrillo), pp. 105–118. Hillsdale, New Jersey: Lawrence Erlbaum Associates.Google Scholar
Chamberlain, S.C. et al., 1994a. Retinal structure in hydrothermal vent shrimp from the Mid-Atlantic Ridge. Society for Neuroscience Abstracts, 20, 132.Google Scholar
Chamberlain, S.C. et al., 1994b. Vision in hydrothermal vent shrimp: unusual structures for seeing in an unusual environment. Annals of Biomedical Engineering, 22, supplement 1, 56.Google Scholar
Clarke, G.L. & Denton, E.J., 1962. Light and animal life. In The sea (ed. M.N, Hill), pp. 456–168. London: 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 de I'lnstitut Océanographique. Monaco, 64, 1–20.Google Scholar
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
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
Hornstein, E.P. & Chamberlain, S.C, 1991. Correlation of photoreceptor structure and lighting environment: implications for photostasis. Society for Neuroscience Abstracts, 17, 298.Google Scholar
Hose, J.E., Martin, G.C. & Gerard, A.S., 1990. A decapod hemocyte classification scheme integrating morphology, cytochemistry, and function. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 166, 265–273.Google Scholar
Johnson, M.L., Shelton, P.M.J., Herring, P.J. & Gardner, S., 1995. Spectral responses from the dorsal organ of a juvenile Rimicaris exoculata from the TAG hydrothermal vent site. BRIDGE Newsletter, 8, 38–42.Google Scholar
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, 397—420.CrossRefGoogle Scholar
Lakin, R.C., Jinks, R.N., Battelle, B-A., Herzog, E.D., Kass, L., Renninger, G.H. & Chamberlain, S.C, 1997. Retinal anatomy of Chorocaris chacei, a deep-sea hydrothermal vent shrimp from the Mid-Atlantic Ridge. Journal of Comparative Neurology, 384, 1–12.Google Scholar
Langmuir, C. et al., 1993. Geological setting and characteristics of the Lucky Strike vent field at 37°17’N on the Mid-Atlantic Ridge. Eos, Transactions of the American Geophysical Union, 74, 99.Google Scholar
Loew, E.R., 1976. Light and photoreceptor degeneration in the Norway Lobster, Nephrops norvegicus (L.). Proceedings of the Royal Society B, 193, 31–44.Google ScholarPubMed
Martin, J.W. & Christiansen, J.C., 1995. A new species of the shrimp genus Chorocaris Martin & Hessler, 1990 (Crustacea: Decapoda: Bresiliidae) from hydrothermal vent fields along the Mid-Atlantic Ridge. Proceedings of the Biological Society of Washington, 108, 220–227.Google Scholar
Meyer-Rochow, V.B., 1981. The eye of Orchomene sp. cf. O. rossi, an amphipod living under the Ross Ice Shelf (Antarctica). Proceedings of the Royal Society, 212, 93–111.Google Scholar
Murton, B.J., 1993. Geological and geochemical investigations between 27°N and 30°N on the Kane-Atlantis segment: the Mid-Atlantic Ridge. Report. Institute of Oceanographic Sciences Deacon Laboratory, no. 236, 33 pp.Google Scholar
Murton, BJ. & Van Dover, C.L., 1993. ALVIN dives on the Broken Spur hydrothermal vent field at 29°10’N on the Mid-Atlantic Ridge. BRIDGE Newsletter, 5, 11–14.Google Scholar
Murton, B.J., Van Dover, C. & Southward, E., 1995. Geological setting and ecology of the Broken Spur hydrothermal vent field: 29°10’N on the Mid-Atlantic Ridge. In Hydrothermal vents and processes (ed. L.M, Parson et al.), pp. 33–41. London: The Geological Society. [Geological Society Special Publication no. 87.]Google Scholar
Nilsson, H.L., 1982. Rhabdom breakdown in the eye of Cirolana borealis (Crustacea) caused by exposure to daylight. Cell and Tissue Research, 227, 633–639.CrossRefGoogle ScholarPubMed
Nilsson, H.L. & Lindström, M., 1983. Retinal damage and sensitivity loss of a light-sensitive crustacean compound eye (Cirolana borealis). Journal of Experimental Biology, 107, 277–292.CrossRefGoogle Scholar
Nuckley, D.J., Jinks, R.N., Battelle, B-A., Herzog, E.D., Kass, L., Renninger, G.H. & Chamberlain, S.C, 1996. Retinal anatomy of a new species of bresiliid shrimp from a hydrothermal vent field on the Mid-Atlantic Ridge. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 190, 98–110.CrossRefGoogle ScholarPubMed
O’Neill, P.J., Jinks, R.N., Herzog, E.D., Battelle, B-A., Kass, L., Renninger, G.H. & Chamberlain, S.C, 1995. The morphology of the dorsal eye of the hydrothermal vent shrimp, Rimicaris exoculata. Visual Neuroscience, 12, 861–875.CrossRefGoogle ScholarPubMed
Pelli, D.G. & Chamberlain, S.C., 1989. The visibility of 350°C black-body radiation by the shrimp Rimicaris exoculata and man. Nature, London, 337, 460–461.CrossRefGoogle Scholar
Rona, P.A., 1992. Deep-sea geysers of the Atlantic. National Geographic, 182, 104–109.Google Scholar
Shelton, P.M., Gaten, J.E. & Chapman, C.J., 1985. Light and retinal damage in Nephrops norvegicus (L.) (Crustacea). Proceedings of the Royal Society B, 226, 217–236.Google Scholar
Tivey, M, Saldanha, L. & Grieve, B., 1993. Alvin dive 2606 summary. In Cruise Report, Lucky Strike/Alvin Expedition (chief scientist C. Langmuir), pp. 21–25. Columbia University, New York: Lamont-Doherty Earth Observatory. [Technical Report No. LDEO-93–2.]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 tell Biology, 106,1151–1160.Google ScholarPubMed
Tunnicliffe, V., 1992. Hydrothermal-vent communities of the deep sea. American Scientist, 80, 336–349.Google Scholar
Tuurala, O. & Lehtinen, A., 1971. Über die Einwirkung von Licht undDunkel auf die Feinstruktur der Lichtsinneszellen der Assel Oniscus asellus L. II. Microvilli und multivesikuläre Körper nach starker Belichtung. Annales Academiae Scienliarum Fennicae A, IV Biologica, 177, 1–8.Google Scholar
Van Dover, C.L., 1995. Ecology of Mid-Atlantic Ridge hydrothermal vents. In Hydrothermal vents and processes (ed. L.M, Parson et al.), pp. 257–289. London: The Geological Society. [Geological Society Special Publication no. 87.]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, London, 337, 458–60.CrossRefGoogle Scholar
Van Dover, C.L. et al., 1994. Light at deep sea hydrothermal vents. Transactions of the 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