Skip to main content
SpringerLink
Log in

Variations of antioxidant enzymes in Daphnia species and populations as related to ambient UV exposure

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

To assess their role in photoprotection in the crustacean zooplankton Daphnia spp., activities of the antioxidants catalase (CAT), superoxide dismutase (SOD), glutathione transferase (GST) and content of carotenoids (CAR) were studied in 4 Daphniaspecies from a total of 50 populations. Included in the survey were alpine and lowland populations of both pigmented and non-pigmented D. longispina, rock-pool and laboratory clones of D. magna and Arctic populations of the D. pulex/D. middendorffianacomplex. Most of the surveyed populations inhabit shallow ponds, and are thus highly exposed to UV-radiation during the summer. The results are primarily discussed in relation to antioxidants as possible protection against UV-radiation. D. pulex, D. middendorffianaand D. longispinaoccurred both as hyaline and pigmented (carapace melanization) morphs. The most notable inter-species differences were the high activity of CAT in the D. magnalab-clone, the low activity of GST in melanic animals from the D. pulexgroup and the high activity of SOD in D. longispinafrom a lowland humic pond. Contrary to expectations, we found no differences in antioxidant capacity between melanic and non-pigmented alpine D. longispina. Intraspecies variation in antioxidant activities was studied in relation to pond characteristics. Among the alpine populations of D. longispina there was a significant positive correlation between absorbance (300 nm) of the pond water and CAT activity, which could be related to ambient levels of photoinduced hydrogen peroxide production in these small water bodies. The data from this comparative study provide insight in photo-protective mechanisms in cladocera, and constitute a valuable basis for future research on pro-oxidant and antioxidant processes in alpine and arctic freshwater zooplankton.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abele, D., B. Burlando, A. Viarengo & H.-O. Pörtner, 1998. Exposure to elevated temperatures and hydrogen peroxide elicits oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna. Comp. Biochem. Physiol. 120B: 425–435.

    Google Scholar 

  • Bertling, C. J., F. Lin & A. W. Girotti, 1996. Role of hydrogen peroxide in the cytotoxic effects of UVA/B radiation on mammalian cells. Photochem. Photobiol. 64: 137–142.

    Google Scholar 

  • Bradford, M. M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.

    Google Scholar 

  • Buchner, T., D. Abele-Oeschger & H. Theede, 1996. Aspects of antioxidant status in the polychaete Arenicola marina: tissue and subcellular distribution, and reaction to environmental hydrogen peroxide and elevated temperatures. Mar. Ecol. Prog. Ser. 143: 141–150.

    Google Scholar 

  • Byron, E. R., 1982. The adaptive significance of calanoid copepod pigmentation: a comparative and experimental analysis. Ecology 63: 1871–1886.

    Google Scholar 

  • Claiborne, A., 1985. Catalase activity. In Greenwald, R. A. (ed.), Handbook of Methods for Oxygen Radical Research. CRC Press, Boca Raton: 283–284.

    Google Scholar 

  • Clarke, A., 1983. Life in cold water: the physiological ecology of polar marine ectotherms. Oceanogr. mar. biol. Ann. Rev. 21: 341–453.

    Google Scholar 

  • Cooper, W. J., D. R. S. Lean & J. H. Carey, 1989. Spatial and temporal patterns of hydrogen peroxide in lake waters. Can. J. Fish. aquat. Sci. 46: 1227–1231.

    Google Scholar 

  • Cossins, A. R. & C. L. Prosser, 1978. Evolutionary adaptations of membranes to temperature. Proc. natl. Acad. Sci. U.S.A. 75: 2040–2043.

    Google Scholar 

  • Dahlback, A., T. Henriksen, S. H. H. Larsen & K. Stamnes, 1989. Biological UV-doses and the effect of an ozon layer depletion. Photochem. Photobiol. 49: 621–625.

    Google Scholar 

  • Dahlback, A. & K. Stamnes, 1991. A new spherical model for computing the radiation field available for photolysis and heating at twilight. Planet Space Sci. 39: 671–683.

    Google Scholar 

  • Di Giulio R. T., P. C. Washburn, R. J. Wenning, G. W. Winston & C. S. Jewell, 1989. Biochemical responses in aquatic animals: a review of determinants of oxidative stress. Environ. Toxicol. Chem. 8: 1103–1123.

    Google Scholar 

  • Fuchs, J. & L. Packer, 1991. Photooxidative stress in the skin. In Sies, H. (ed.), Oxidative Stress: Oxidants and Antioxidants. Academic Press, London: 559–583.

    Google Scholar 

  • Fuchs J., M. E. Huflejt, L. M. Rothfuss, D. S. Wilson, G. Carcamo & L. Packer, 1989. Impairment of enzymic and nonenzymic antioxidants in skin by UVB irradiation. J. Invest. Dermatol. 93: 769–773.

    Google Scholar 

  • Green J., 1957. Carotenoids in Daphnia. Proc. r. Soc. London Ser. B 147: 392–401.

    Google Scholar 

  • Habig, W. H., M. J. Pabst & W. B. Jakoby, 1974. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249: 7130–7139.

    Google Scholar 

  • Hairston, N. G. Jr., 1978. Carotenoid photoprotection in Diaptomus kenai. Verh. int. Ver. Limnol. 20: 2541–2545.

    Google Scholar 

  • Hairston, N. G. Jr., 1979. The adaptive significance of color polymorphism in two species of Diaptomus (Copepoda). Limnol. Oceanogr. 24: 15–37.

    Google Scholar 

  • Hairston, N. G. Jr., 1981. The interaction of salinity, predators, light and copepod color. Hydrobiologia 81: 151–158.

    Google Scholar 

  • Halliwell, B. & J. M. C. Gutteridge, 1986. Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Arch. Biochem. Biophys. 246: 501–514.

    Google Scholar 

  • Hebert, P. D. N. & C. J. Emery, 1990. The adaptive significance of cuticular pigmentation in Daphnia. Funct. Ecol. 4: 703–710.

    Google Scholar 

  • Hessen, D. O., 1993. DNA-damage and pigmentation in alpine and arctic zooplankton as bioindicators of UV-radiation. Verh. int. Ver. Limnol. 25: 482–486.

    Google Scholar 

  • Hessen, D. O., 1994. Daphnia responses to UV-light. Arch. Hydrobiol. Beih. Ergebn. Limnol. 43: 185–195.

    Google Scholar 

  • Hessen, D. O., 1996. Competitive trade-off strategies in Arctic Daphnia linked to melanism and UV-B stress. Polar Biol. 16: 573–579.

    Google Scholar 

  • Hessen, D. O. & K. Sørensen, 1990. Photoprotective pigmentation in alpine zooplankton populations. Aqua Fenn. 20: 165–170.

    Google Scholar 

  • Hessen, D. O., H. J. De Lange & E. Van Donk, 1997. UVinduced changes in phytoplankton cells and its effects on gazers. Freshwat. Biol. 38: 513–524.

    Google Scholar 

  • Hessen, D. O., J. Borgeraas, K. Kessler & U. H. Refseth, 1999. UV-B susceptibility and photoprotection of Arctic Daphnia morphotypes. Polar Res. 18: 345–352.

    Google Scholar 

  • Hiratsuka, A., H. Saito, K. Hirose & T. Watabe, 1999. Marked expression of glutathione S-transferase A4-4 detoxifying 4-hydroxy-2(E)-nonenal in the skin of rats irradiated by ultraviolet B-band light (UVB). Biochem. Biophys. Res. Commun. 260: 740–746.

    Google Scholar 

  • Hobæk, A. & H. G. Wolf, 1991. Ecological genetics of Norwegian Daphnia. II. Distribution of Daphnia longispina genotypes in relation to short-wave radiation and water colour. Hydrobiologia 225: 229–243.

    Google Scholar 

  • Karentz, D., 1994. Ultraviolet tolerance mechanisms in Antarctic marine organisms. In Weiler, C. A. & P. A. Penhale (eds), Ultraviolet Radiation in Antarctica: Measurements and Biological Effects. Antarctic Research Series, Vol. 62. American Geophysical Union, Washington DC: 93–110.

    Google Scholar 

  • Kerb, R., J. Brockmöller, T. Reum & I. Roots, 1997. Deficiency of glutathione S-transferases T1 and M1 as heritable factors of increased cutaneous UV sensitivity. J. Invest. Dermatol. 108: 229–232.

    Google Scholar 

  • Kerr, J. B. & C. T. McElroy, 1993. Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion. Science 262: 1032–1034.

    Google Scholar 

  • Ketterer, B. & D. J. Meyer, 1989. Glutathione transferases: a possible role in the detoxication and repair of DNA and lipid hydroperoxides. Mutat. Res. 214: 33–40.

    Google Scholar 

  • Kirk, J. T. O., 1994. Optics of UV-B radiation in natural waters. Arch. Hydrobiol. Beih. Ergebn. Limnol. 43: 1–16.

    Google Scholar 

  • Krinsky, N. I., 1993. Actions of carotenoids in biological systems. Annu. Rev. Nutr. 13: 561–587.

    Google Scholar 

  • LeBlanc, G. A. & B. J. Cochrane, 1987. Identification of multiple glutathione S-transferases from Daphnia magna. Comp. Biochem. Physiol. 88B: 39–45.

    Google Scholar 

  • Luecke, C. & W. J. O'Brien, 1983. Photoprotective pigments in a pond morph of Daphnia middendorffiana. Arctic 36: 365–368.

    Google Scholar 

  • Malloy, K. D., M. A. Holman, D. Mitchell & H. W. Detrich III, 1997. Solar UVB-induced DNA damage and photoenzymatic DNA repair in antarctic zooplankton. Proc. natl. Acad. Sci. U.S.A. 94: 1258–1263.

    Google Scholar 

  • Masaki, H., T. Atsumi & H. Sakurai, 1995. Detection of hydrogen peroxide and hydroxyl radicals in murine skin fibroblasts under UVB irradiation. Biochem. Biophys. Res. Commun. 206: 474–479.

    Google Scholar 

  • McKinley, A. F. & B. L. Diffey, 1987. A reference action spectrum for ultraviolet induced erythema on human skin. Commission Internationale de l'Eclaire: 17–22.

  • Morrill, A. C., E. N. Powell, R. R. Bidigare & J. M. Shick, 1988. Adaptations to life in the sulfide system: a comparison of oxygen detoxifying enzymes in thiobiotic and oxybiotic meiofauna (and freshwater planarians). J. Comp. Physiol. B 158: 335–344.

    Google Scholar 

  • Morris, D. P., H. Zagarese, C. E. Williamson, E. G. Balseiro, B. R. Hargreaves, B. Modenutti, R. Moeller & C. Queimalinos, 1995. The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnol. Oceanogr. 40: 1381–1391.

    Google Scholar 

  • Murali, N. S., A. H. Teramura & S. K. Randall, 1988. Response differences between two soybean cultivars with contrasting UVB radiation sensitivities. Photochem. Photobiol. 48: 653–657.

    Google Scholar 

  • Schindler, D. W., P. J. Curtis, B. R. Parker & M. P. Stainton, 1996. Consequences of climate warming and lake acidification for UVB penetration in North American boreal lakes. Nature 379: 705–708.

    Google Scholar 

  • Scully, N. M., D. J. McQueen & D. R. S. Lean, 1996. Hydrogen peroxide formation: the interaction of ultraviolet radiation and dissolved organic carbon in lake waters along a 43-75°. N gradient. Limnol. Oceanogr. 41: 540–548.

    Google Scholar 

  • Scully, N. M., W. F. Vincent, D. R. S. Lean & W. J. Cooper, 1997. Implications of ozone depletion for surface-water photochemistry: sensitivity of clear lakes. Aquat. Sci. 59: 260–274.

    Google Scholar 

  • Shindo, Y. & T. Hashimoto, 1995. Antioxidant defence mechanism of the skin against UV irradiation: study of the role of catalase using acatalasaemia fibroblasts. Arch. Dermatol. Res. 287: 747–753.

    Google Scholar 

  • Shindo, Y., E. Witt, D. Han & L. Packer, 1994. Dose-response effects of acute ultraviolet irradiation on antioxidants and molecular markers of oxidation in murine epidermis and dermis. J. Invest. Dermatol. 102: 470–475.

    Google Scholar 

  • Siebeck, O., 1978. Ultraviolet tolerance of planktonic crustaceans. Verh. int. Ver. Limnol. 20: 2469–2473.

    Google Scholar 

  • Siebeck, O. & U. Böhm, 1991. UV-B effects on aquatic animals. Verh. int. Ver. Limnol. 24: 2773–2777.

    Google Scholar 

  • Siebeck, O. & U. Böhm, 1994. Challenges for an appraisal of UVB effects upon planktonic crustaceans under natural radiation conditions with a non-migrating (Daphnia pulex obtusa) and a migrating cladoceran (Daphnia galeata). Arch. Hydrobiol. Beih. Ergebn. Limnol. 43: 197–206.

    Google Scholar 

  • Spitz, D. R. & L. W. Oberley, 1989. An assay for superoxide dismutase activity in mammalian tissue homogenates. Anal. Biochem. 179: 8–18.

    Google Scholar 

  • Storelli, C., R. Acierno & M. Maffia, 1998. Membrane lipid and protein adaptations in Antarctic fish. In Pörtner, H. O. & R. C. Playle (eds), Cold Ocean Physiology. Soc. Exp. Biol. Seminar Ser. 66, Cambridge University Press, Cambridge: 166–189.

    Google Scholar 

  • Storz, U. C. & R. J. Paul, 1998. Phototaxis in water fleas (Daphnia magna) is differently influenced by visible and UV light. J. Comp. Physiol. A 183: 709–717.

    Google Scholar 

  • Vega, M. P. & R. A. Pizarro, 2000. Oxidative stress and defence mechanisms of the freshwater cladoceran Daphnia longispina exposed to UV radiation. J. Photochem. Photobiol. B: Biol. 54: 121–125.

    Google Scholar 

  • Viarengo, A., D. Abele-Oeschger & B. Burlando, 1998. Effects of low temperature on prooxidant processes and antioxidant defence systems in marine organisms. In Pörtner, H. O. & R. C. Playle (eds), Cold Ocean Physiology. Soc. Exp. Biol. Seminar Ser. 66, Cambridge University Press, Cambridge: 212–235.

    Google Scholar 

  • Wang, P. & H. E. Schellhorn, 1995. Induction of resistance to hydrogen peroxide and radiation in Deinococcus radiodurans. Can. J. Microbiol.41: 170–176.

    Google Scholar 

  • Weider, L. J. & P. D. N. Hebert, 1987. Ecological and physiological differentiation among low-Arctic clones of Daphnia pulex. Ecology 68: 188–198.

    Google Scholar 

  • Williamson, C. E., H. E. Zagarese, P. C. Schulze, B. R. Hargreaves & J. Seva, 1994. The impact of short-term exposure to UV-B radiation on zooplankton communities in north temperate lakes. J. Plankton Res. 16: 205–218.

    Google Scholar 

  • Yasui, H. & H. Sakurai, 2000. Chemiluminescent detection and imaging of reactive oxygen species in live mouse skin exposed to UVA. Biochem. Biophys. Res. Commun. 269: 131–136.

    Google Scholar 

  • Zellmer, I. D., 1995. UV-B-tolerance of alpine and arctic Daphnia. Hydrobiologia 307: 153–159.

    Google Scholar 

  • Zigman, S., J. Reddan, J. B. Schultz & T. McDaniel, 1996. Structural and functional changes in catalase induced by near-UV radiation. Photochem. Photobiol. 63: 818–824.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Section of Limnology, University of Oslo, P.O. Box 1027, Blindern, N-0316, Oslo, Norway

    Jan Borgeraas

Authors
  1. Jan Borgeraas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dag O. Hessen
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Borgeraas, J., Hessen, D.O. Variations of antioxidant enzymes in Daphnia species and populations as related to ambient UV exposure. Hydrobiologia 477, 15–30 (2002). https://doi.org/10.1023/A:1021056409446

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1021056409446

Search

Navigation