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Visual pigment, dark adaptation and rhodopsin renewal in the eye of Pontoporeia affinis (Crustacea, Amphipoda)

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Abstract

The benthic amphipod Pontoporeia affinis lives in the Baltic sea and in northern European lakes in an environment where very little light is available for vision. The eyes, consisting of 40–50 ommatidia, are correspondingly modified. Microspectrophotometric recordings on isolated eyes show the presence of at least two kinds of screening pigments in the ommatidia with maxima at 540–580 nm and 460–500 nm. Difference spectra obtained from the rhabdoms after exposure to red and blue light, respectively, give evidence of a single rhodopsin with its maximum at 548 nm and a 500-nm metarhodopsin. In ERG recordings sensitivity in the dark-adapted state, after saturating exposures to blue and to red light, stabilizes at levels determined by the rhodopsin concentration. No change is observed during 10–14 h after the beginning of dark adaptation. However, using animals pre-exposed with a strong red light and then kept in darkness, it is found that after a delay of 20–40 h sensitivity of the dark-adapted eye begins to increase and finally, after 5–6 days reaches a level corresponding to 100% rhodopsin. Thus, a slow renewal of rhodopsin appears to occur in darkness, where a photoisomerization of metarhodopsin is excluded.

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Abbreviations

ERG:

electroretinogram

IR:

infrared

MSP:

microspectrophotometry

References

  • Almagor E, Hillman P, Minke B (1979) Upper limit on translational diffusion of visual pigment in intact unfixed barnacle photoreceptors. Biophys Struct Mech 5:243–248

    Google Scholar 

  • Arikawa K, Kawamata K, Suzuki T, Eguchi E (1987) Daily changes of structure, function and rhodopsin content in the compound eye of the crab Hemigrapsus sanguineus. J Comp Physiol A 161:161–174

    Google Scholar 

  • Barnes SN, Goldsmith TH (1977) Dark adaptation, sensitivity and rhodopsin level in the eye of the lobster, Homarus. J Comp Physiol 120:143–159

    Google Scholar 

  • Beatty RA (1949) The pigmentation of cavernicolous animals. III. The carotenoid pigments of some amphipod Crustacea. J Exp Biol 26:125–130

    Google Scholar 

  • Blest AD, Maples J (1979) Exocytotic shedding and glial uptake of photoreceptor membrane by a salticid spider. Proc R Soc Lond 8204:105–112

    Google Scholar 

  • Bridges CDB (1972) The rhodopsin-porphyropsin visual system. In: Dartnall HJA (ed) Photochemistry of vision (Handbook of sensory physiology, vol VII/1). Springer, Berlin Heidelberg New York, pp 417–480

    Google Scholar 

  • Briggs MH (1961) Visual pigment of grapsoid crabs. Nature 190:784–786

    Google Scholar 

  • Bruno MS, Barnes SN, Goldsmith TH (1977) The visual pigment and visual cycle of the lobster, Homarus. J Comp Physiol 120:123–142

    Google Scholar 

  • Cronin TW, Forward RB Jr (1988) The visual pigments of crabs. I. Spectral characteristics. J Comp Physiol A 162:463–478

    Google Scholar 

  • Cronin TW, Goldsmith TH (1984) Dark regeneration of rhodopsin in crayfish photoreceptors. J Gen Physiol 84:63–81

    Google Scholar 

  • Debaisieux P (1944) Les yeux des Crustaces. La Cellule 50:9–122

    Google Scholar 

  • Denton EJ, Warren FJ (1957) The photosensitive pigments in the retinae of deep-sea fish. J Mar Biol Assoc UK 36:651–662

    Google Scholar 

  • Donner KO (1971) On vision in Pontoporeia affinis and P. femorata (Crustacea, Amphipoda). Commentat Biol 41:1–17

    Google Scholar 

  • Donner KO, Lindström M (1980) Sensitivity to light and circadian activity of Pontoporeia affinis (Crustacea, Amphipoda). Ann ZoolFenn 17:203–212

    Google Scholar 

  • Ebrey TG, Honig B (1977) New wavelength dependent visual pigment nomograms. Vision Res 17:147–151

    Google Scholar 

  • Eguchi E, Waterman TH (1967) Changes in the retinal fine structure induced in the crab Libinia by light and dark adaptation. Z Zellforsch 79:209–229

    Google Scholar 

  • Eguchi E, Waterman TH (1976) Freeze-etch and histochemical evidence for cycling in crayfish photoreceptor membranes. Cell Tissue Res 169:419–434

    Google Scholar 

  • Elofsson R, Hallberg E (1973) Correlation of ultrastructure and chemical composition of crustacean chromatophore pigment. J Ultrastruct Res 44:421–429

    Google Scholar 

  • Fernandez HR (1973) Spectral sensitivity and visual pigment of the compound eye of the galatheid crab Pleuroncodes planipes. Mar Biol 20:148–153

    Google Scholar 

  • Forward RB Jr, Cronin TW, Douglass JK (1988) The visual pigments of crabs. II. Environmental adaptations. J Comp Physiol A 162:479–490

    Google Scholar 

  • Goldsmith TH (1972) The natural history of invertebrate visual pigments. In: Dartnall HJA (ed) Photochemistry of vision (Handbook of sensory physiology, vol VII/1). Springer, Berlin Heidelberg New York, pp 685–719

    Google Scholar 

  • Goldsmith TH (1978) The effects of screening pigments on the spectral sensitivity of some Crustacea with scotopic (superposition) eyes. Vision Res 18:475–482

    Google Scholar 

  • Goldsmith TH, Wehner R (1977) Restrictions on rotational and translational diffusion of pigment in the membranes of a rhabdomeric photoreceptor. J Gen Physiol 70:453–490

    Google Scholar 

  • Green JB (1972) Pigmentation of the eyes of Nebalia bipes Fabr. (Leptostraca). Crustaceana 22:206–207

    Google Scholar 

  • Hafner GS, Tokarski TR (1988) The diurnal pattern of protein and photopigment synthesis in the retina of the crayfish, Procambarus clarkii. J Comp Physiol A 163:253–258

    Google Scholar 

  • Hafner GS, Tokarski T, Jones C, Martin R (1982) Rhabdom degradation in white-eyed and wild-type crayfish after long term dark adaptation. J Comp Physiol 148:419–429

    Google Scholar 

  • Hallberg E, Elofsson R (1989) Construction of the pigment shield of the crustacean compound eye: a review. J Crust Biol 9:359–372

    Google Scholar 

  • Hallberg E, Nilsson HL, Elofsson R (1980) Classification of amphipod compound eyes — the fine structure of the ommatidial units (Crustacea, Amphipoda). Zoomorphol 94:279–306

    Google Scholar 

  • Hamdorf K (1979) The physiology of invertebrate visual pigments. In: Autrum H (ed) Invertebrate photoreceptors (Handbook of sensory physiology, vol VII/6). Springer, Berlin Heidelberg New York, pp 145–224

    Google Scholar 

  • Hamdorf K, Schwemer J (1975) Photoregeneration and the adaptation process in insect photoreceptors. In: Snyder AW, Menzel R (eds) Photoreceptor optics. Springer, Berlin Heidelberg New York, pp 263–289

    Google Scholar 

  • Hamdorf K, Paulsen R, Schwemer J (1973) Photoregeneration and sensitivity control of photoreceptors of invertebrates. In: Langer H (ed) Biochemistry and physiology of visual pigments. Springer, Berlin Heidelberg New York, pp 155–166

    Google Scholar 

  • Henning U, Langer H (1986) Untersuchungen zum Turnover der Photorezeptormembran im Auge der Krabbe Ocypode ryderi. Verh Dtsch Zool Ges 79:213

    Google Scholar 

  • Hiller-Adams P, Widder EA, Case JF (1988) The visual pigments of four deep-sea crustacean species. J Comp Physiol A 163:63–72

    Google Scholar 

  • Hillman P, Hochstein S, Minke B (1983) Transduction in invertebrate photoreceptors: role of pigment bistability. Physiol Rev 63:668–772

    Google Scholar 

  • Itaya SJ (1976) Rhabdom changes in the shrimp, Palaemonetes. Cell Tissue Res 166:265–273

    Google Scholar 

  • Langer H (1975) Properties and functions of screening pigments in insect eyes. In: Snyder AW, Menzel R (eds) Photoreceptor optics. Springer, Berlin Heidelberg New York, pp 429–455

    Google Scholar 

  • Langer H, Schlecht P, Schwemer J (1982) Microspectrophotometric investigation of insect visual pigments. In: Parker L (ed) Methods in enzymology, vol 81. Academic Press, New York, pp 729–741

    Google Scholar 

  • Langer H, Pieper M, Henning U (1990) Photoreceptor membranes and visual pigments in the apposition eyes of the terrestrial crab Ocypode ryderi (Ocypodidae) during the daily light cycle. (Proc Internat Crust Conf, Brisbane). Mem Queensland Mus 31:279

    Google Scholar 

  • Lindström M, Nilsson HL (1983) Spectral and visual sensitivities of Cirolana borealis Lilljeborg, a deep-water isopod (Crustacea: Flabellifera). J Exp Mar Biol Ecol 69:243–256

    Google Scholar 

  • Lindström M, Nilsson HL (1988) Eye function of Mysis relicta Lovén (Crustacea) from two photic environments. Spectral sensitivity and light tolerance. J Exp Mar Biol Ecol 120:23–37

    Google Scholar 

  • Lindström M, Nilsson HL, Meyer-Rochow VB (1988) Recovery from light-induced sensitivity loss in the eye of the crustacean Mysis relicta in relation to temperature: a study of ERG-determined V÷log I relationships and morphology at 4 °C and 14 °C. Zool Sci 5:743–757

    Google Scholar 

  • Lipetz LE, Cronin TW (1988) Application of an invariant spectral form to the visual pigments of crustaceans: implications regarding the binding of the chromophore. Vision Res 28:1083–1093

    Google Scholar 

  • Loew ER (1976) Light and photoreceptor degeneration in the Norway lobster, Nephrops norvegicus (L.). Proc R Soc Lond B 193:31–44

    Google Scholar 

  • Makino-Tasaka M, Suzuki T (1986) Quantitative analysis of retinal and 3-dehydroretinal by high-pressure liquid chromatography. Methods Enzymol 123:53–61

    Google Scholar 

  • Meyer-Rochow VB (1981) The eye of Orchomene sp. cf. O. rossi, an amphipod living under the Ross Ice Shelf (Antarctica). Proc R Soc Lond B 212:93–111

    Google Scholar 

  • Michel A, Anders F (1954) Über die Pigmente im Auge von Gammarus pulex L. (Crust., Amphipod.). Naturwissenschaften 41:72

    Google Scholar 

  • Minke B, Kirschfeld K (1978) Microspectrophotometric evidence for two photointerconvertible States of visual pigment in the barnacle lateral eye. J Gen Physiol 71:37–45

    Google Scholar 

  • Nässei DR, Waterman TH (1979) Massive diurnally modulated membrane turnover in crab light and dark adaptation. J Comp Physiol 131:205–216

    Google Scholar 

  • Parker GH (1899) The photomechanical changes in the retinal pigment of Gammarus. Bull Mus Comp Zool Harvard Coll 35:143–150

    Google Scholar 

  • Rosenberg J, Langer H (1993) Feinstruktur der Komplexaugen von Pontoporeia affinis (Amphipoda, Gammaridae) und die Wirkung von Licht auf die Rhabdome. Contrib 6th meeting of German Crustaceologists, Rostock-Warnemünde 1993

  • Schlecht P, Hamdorf K, Langer H (1978) The arrangement of colour receptors in a fused rhabdom of an insect. J Comp Physiol 123:239–243

    Google Scholar 

  • Schwemer J (1983) Pathways of visual pigment regeneration in fly photoreceptor cells. Biophys Struct Mech 9:287–298

    Google Scholar 

  • Schwemer J (1984) Renewal of visual pigment in photoreceptors of the blowfly. J Comp Physiol A 154:535–547

    Google Scholar 

  • Schwemer J (1986) Turnover of photoreceptor membrane and visual pigment in invertebrates. In: Stieve H (ed) The molecular mechanism of photoreception. Dahlem Konf 1985. Springer, Berlin Heidelberg New York, pp 303–326

    Google Scholar 

  • Schwemer J (1989) Visual pigments of compound eyes structure, photochemistry, and regeneration. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Berlin Heidelberg New York, pp 112–133

    Google Scholar 

  • Schwemer J, Langer H (1982) Insect visual pigments. In: Parker L (ed) Methods in enzymology, vol 81. Academic Press, New York, pp 182–197

    Google Scholar 

  • Segerstråle S (1957) On the immigration of the glacial relicts of Northern Europe, with remarks on their prehistory. Commentat Biol 16:1–117

    Google Scholar 

  • Smith WC, Goldsmith TH (1991) The role of retinal photoisomerase in the visual cycle of the honeybee. J Gen Physiol 97:143–165

    Google Scholar 

  • Stavenga DG (1989) Pigments in compound eyes. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Berlin Heidelberg New York, pp 152–172

    Google Scholar 

  • Stavenga DG, Schwemer J (1984) Visual pigments of invertebrates. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum Press, Oxford New York, pp 11–61

    Google Scholar 

  • Stein PJ, Brammer JD, Ostroy SE (1979) Renewal of opsin in the photoreceptor cells of the mosquito. J Gen Physiol 74:565–582

    Google Scholar 

  • Stowe S (1980) Rapid synthesis of photoreceptor membrane and assembly of new microvilli in a crab at dusk. Cell Tissue Res 211:419–440

    Google Scholar 

  • Stowe S (1981) Effects of illumination changes on rhabdom synthesis in a crab. J Comp Physiol 142:19–25

    Google Scholar 

  • Stowe S, de Couet H-G, Davis D (1990) Photoreceptor membrane turnover in the crayfish Cher ax destructor: electron microscopy and anti-rhodopsin electronmicroscopic immunocytochemistry. Cell Tissue Res 262:483–499

    Google Scholar 

  • Suzuki T, Makino-Tasaka M, Eguchi E (1984) 3-dehydroretinal (vitamin A2 aldehyde) in crayfish eye. Vision Res 24:783–787

    Google Scholar 

  • Uitto A, Sarvala J (1991) Seasonal growth of the benthic aphipods Pontoporeia affinis and P. femorata in a Baltic archipelago in relation to environmental factors. Mar Biol 111:237–246

    Google Scholar 

  • Waldron KD (1953) A new subspecies of Pontoporeia affinis in Lake Washington, with a discussion of its morphology and life cycle. M.S. Thesis, University of Washington, USA

    Google Scholar 

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Donner, K.O., Langer, H., Lindström, M. et al. Visual pigment, dark adaptation and rhodopsin renewal in the eye of Pontoporeia affinis (Crustacea, Amphipoda). J Comp Physiol A 174, 451–459 (1994). https://doi.org/10.1007/BF00191711

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