Skip to main content

Growth kinetics related to physiological parameters in young Saccorhiza dermatodea and Alaria esculenta sporophytes exposed to UV radiation

Abstract

Young sporophytes of Saccorhiza dermatodea and Alaria esculenta cultured from Spitsbergen isolates were exposed in the laboratory to either only photosynthetically active radiation (PAR) or to a spectrum including UV-radiation (PAR+UVA+UVB) by use of cutoff glass filters. The plants were grown at 8±2°C and 16:8 h light–dark cycles with 6 h additional UV exposure in the middle of the light period. Growth was measured every 10 min using growth chambers with online video measuring technique for 18–21 days. Tissue morphology and absorption spectra were measured in untreated young sporophytes while tissue chlorophyll-a content and DNA damage were measured from treated thalli at the end of the experiment. Under UVR, growth rates of S. dermatodea were significantly reduced while A. esculenta have a potential to acclimate. Tissue chlorophyll-a contents in both species were not significantly different between treatments suggesting that these algae may acclimate to moderate UVR fluence. Higher DNA damage in S. dermatodea effectively diverted photosynthetic products for repair constraining growth. Tissue optics (opacity and translucence) was correlated to the tissue absorbance in the UVR region characteristics of phlorotannin, an important UV-absorbing compound in brown macroalgae. Growth rates of sporophytes of both species exposed to PAR without UV was similar during day and night. The results showed that both species can recruit and inhabit a similar coastal zone when appropriate strategies are expressed to minimize damage in response to the stress factor.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Aguilera J, Karsten U, Lippert H, Vögele B, Philipp E, Hanelt D, Wiencke C (1999) Effects of solar radiation on growth, photosynthesis and respiration of marine macroalgae from the Arctic. Mar Ecol Prog Ser 191:109–119

    Google Scholar 

  2. Aguilera J, Bischof K, Karsten U, Hanelt D, Wiencke C (2002) Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. II. Pigment accumulation and biochemical defence systems against high light stress. Mar Biol 140:1087–1095

    Google Scholar 

  3. Altamirano M, Flores-Moya A, Figueroa F-L (2000) Long-term effects of natural sunlight under various ultraviolet radiation conditions on growth and photosynthesis of intertidal Ulva rigida (Chlorophyceae) cultivated in situ. Bot Mar 43:19–26

    Google Scholar 

  4. Apprill AM, Lesser MO (2003) Effects of ultraviolet radiation on Laminaria saccharina in relation to depth and tidal height in the Gulf of Maine. Mar Ecol Prog Ser 256:75–85

    Google Scholar 

  5. Bischof K, Hanelt D, Tüg H, Karsten U, Brouwer PEM, Wiencke C (1998) Acclimation of brown algal photosynthesis to ultraviolet radiation in Arctic coastal waters (Spitsbergen, Norway). Polar Biol 20:388–395

    Google Scholar 

  6. Bischof K, Hanelt D, Wiencke C (1999): Acclimation of maximal quantum yield of photosynthesis in the brown alga Alaria esculenta under high light and UV radiation. Plant Biol 1:435–444

    Google Scholar 

  7. Bischof K, Hanelt D, Aguilera J, Karsten U, Vögele B, Sawall T, Wiencke C (2002a) Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. I. Sensitivity of photosynthesis to ultraviolet radiation. Mar Biol 140:1097–1106

    Google Scholar 

  8. Bischof K, Kräbs G, Wiencke C, Hanelt D (2002b) Solar ultraviolet radiation affects the activity of ribulose-1,5-biphosphate carboxylase-oxygenase and the composition of photosynthetic and xanthophyll cycle pigments in the intertidal green alga Ulva lactuca L. Planta 215:502–509

    Google Scholar 

  9. Caldwell MM (1971) Solar ultraviolet radiation and the growth and development of higher plants. In: Giese AC (ed) Photophysiology. Academic, New York, pp 131–177

    Google Scholar 

  10. Caldwell MM, Robberecht R, Flint SD (1983) Internal filters: prospects for UV-acclimation in higher plants. Physiol Plant 58:445–450

    Google Scholar 

  11. Clendennen SK, Zimmerman RC, Powers DA, Alberte RS (1996) Photosynthetic response of giant kelp Macrocystis pyrifera (Phaeophyceae) to ultraviolet radiation. J Phycol 32:614–620

    Google Scholar 

  12. Coelho SM, Rijstenbil JW, Brown MT (2000) Impacts of anthropogenic stresses on the early development stages of seaweeds. J Aquat Ecosyst Stress Recovery 7:317–333

    Google Scholar 

  13. Dring MJ, Makarov V, Schoschina E, Lorenz M, Lüning K (1996) Influence of ultraviolet-radiation on chlorophyll fluorescence and growth in different life-history stages of three species of Laminaria (Phaeophyta). Mar Biol 126:183–191

    Google Scholar 

  14. Dummermuth AL, Wiencke C (2003) Experimental investigation of seasonal development in six Antarctic red macroalgae. Antarct Sci 15:449–457

    Google Scholar 

  15. Franklin LA, Forster RM (1997) The changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology. Eur J Phycol 32: 207–232

    Google Scholar 

  16. Garcia-Pichel F. (1994) A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnol Oceanogr 39:1704–1717

    Google Scholar 

  17. Granbom M, Pedersén M, Kadel P, Lüning K (2001) Circadian rhythm of photosynthetic oxygen evolution in Kappaphycus alvarezii (Rhodophyta): dependence on light quantity and quality. J Phycol 37:1020–1025

    Google Scholar 

  18. Han T, Kain J.M. (1996). Effect of photon irradiance and photoperiod on young sporophytes of four species of the Laminariales. Eur J Phycol 31:233–240

    Google Scholar 

  19. Hanelt D, Melchersmann B, Wiencke C, Nultsch W (1997a) Effects of high light stress on photosynthesis of polar macroalgae in relation to depth distribution. Mar Ecol Prog Ser 149:255–266

    Google Scholar 

  20. Hanelt D, Wiencke C, Nultsch W (1997b) Influence of UV radiation on photosynthesis of Arctic macroalgae in the field. J Photochem Photobiol B Biol 38:40–47

    Google Scholar 

  21. Hanelt D, Wiencke C, Karsten U, Nultsch W (1997c) Photoinhibition and recovery after high light stress in different developmental and life-history stages of Laminaria saccharina (Phaeophyta). J Phycol 33:387–395

    Google Scholar 

  22. Hanelt D, Tüg GH, Bischof K, Groß C, Lippert H, Sawall T, Wiencke C (2001) Light regime in an Arctic fjord: a study related to stratospheric ozone depletion as a basis for determination of UV effects on algal growth. Mar Biol 138:649–658

    Google Scholar 

  23. Henry BE, Van Alstyne KL (2004) Effects of UV radiation on growth and phlorotannins in Fucus gardneri (Phaeophyceae) juveniles and embryos. J Phycol 40:527–533

    Google Scholar 

  24. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  25. Huovinen PS, Oikari AOJ, Soimasuo MR, Cherr GN (2000) Impact of UV radiation on the early development of the giant kelp (Macrocystis pyrifera) gametophytes. Photochem Photobiol 72:308–313

    Google Scholar 

  26. Jacobsen S, Lüning K, Goulard F (2003) Cicadian changes in relative abundance of two photosynthetic transcripts in the marine macroalga Kappaphycus alvarezii (Rhodophyta). J Phycol 39:888–896

    Google Scholar 

  27. Johansson G, Snoeijs P (2002) Macroalgal photosynthetic responses to light in relation to thallus morphology and depth zonation. Mar Ecol Prog Ser 244:63–72

    Google Scholar 

  28. Jokela K, Leszczynski K, Visuri R (1993) Effects of Arctic ozone depletion and snow on UV exposure in Finland. Photochem Photobiol 58:559–566

    Google Scholar 

  29. Kain JM (1989) The seasons in the subtidal. Br Phycol J 24:203–215

    Google Scholar 

  30. Karentz D (1994) Ultraviolet tolerance mechanisms in Antarctic marine organisms. In: Weiler CS, Penhale PA (eds) Ultraviolet radiation in Antarctica: Measurements and Biological effects (Antarctic Research Series no. 62). American Geophysical Union, Washington DC, pp 93–110

    Google Scholar 

  31. Karsten U, Bischof K, Wiencke C (2001) Photosynthetic performance of Arctic macroalgae after transplantation from deep to shallow waters followed by exposure to natural solar radiation. Oecologia 127:11–20

    Google Scholar 

  32. Lüder UH, Knoetzel J, Wiencke C (2001) Acclimation of photosynthesis and pigments to seasonally changing light conditions in the endemic Antarctic red macroalga Palmaria decipiens. Polar Biol 24:598–603

    Google Scholar 

  33. Lüder UH, Wiencke C, Knoetzel J (2002) Acclimation of photosynthesis and pigments during and after six months of darkness in Palmaria decipiens (Rhodophyta): a study to simulate Antarctic winter sea ice cover. J Phycol 38:904–913

    Google Scholar 

  34. Lüning K (1979) Growth strategies of three Laminaria species (Phaeophyceae) inhabiting different depth zones in the sublittoral region of Helgoland (North Sea). Mar Ecol Prog Ser 1:195–207

    Google Scholar 

  35. Lüning K (1985) Meeresbotanik: Verbreitung, Ökophysiologie und Nutzung der marine Makroalgen. Georg Thieme Verlag, Stuttgart, pp 375

    Google Scholar 

  36. Lüning K (1992) Day and night kinetics of growth rate in green, brown, and red seaweeds. J Phycol 28:794–803

    Google Scholar 

  37. Lüning K (1993) Environmental and internal control of seasonal growth in seaweeds. Hydrobiologia 260/261:1–14

    Google Scholar 

  38. Lüning K (1994a) Circadian growth rhythm in juvenile sporophytes of Laminariales (Phaeophyta). J Phycol 30:193–199

    Google Scholar 

  39. Lüning K (1994b) When do algae grow? The third founders’ lecture. Eur J Phycol 29:61–67

    Google Scholar 

  40. Lüning K (2001) Circadian growth in Porphyra umbilicalis (Rhodophyta): spectral sensitivity of the circadian system. J Phycol 37:52–58

    Google Scholar 

  41. Makarov MV, Voskoboinikov GM (2001) The influence of ultraviolet-B radiation on spore resease and growth of the kelp Laminaria saccharina. Bot Mar 44:89–94

    Google Scholar 

  42. Michler T, Aguilera J, Hanelt D, Bischof K, Wiencke C (2002) Long-term effects of ultraviolet radiation on growth and photosynthetic performance of polar and cold-temperate macroalgae. Mar Biol 140:1117–1127

    Google Scholar 

  43. Müller R, Crutzen PJ, Grooß JU, Brühl C, Russel JM, Gernandt H, Mc Kenna DS, Tuck AF (1997) Severe ozone loss in the Arctic during the winter of, 1995–96. Nature 389:709–712

    Google Scholar 

  44. Pakker H, Beekman CAC, Breeman AM (2000a) Efficient photoreactivation of UVBR-induced DNA damage in the sublittoral macroalga Rhodymenia pseudopalmata (Rhodophyta). Eur J Phycol 35:109–114

    Google Scholar 

  45. Pakker H, Martins RST, Boelen P, Buma AGJ, Nikaido O, Breeman AM (2000b) Effects of temperature on the photoreactivation of ultraviolet-B-induced DNA damage in Palmaria palmata (Rhodophyta). J Phycol 36:334–341

    Google Scholar 

  46. Pavia H, Brocks E (2000) Extrinsic factors influencing phlorotannin production in the brown alga Ascophyllum nodosum. Mar Ecol Prog Ser 193:285–294

    Google Scholar 

  47. Pavia H, Cervin G, Lindgren A, Åberg P (1997) Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar Ecol Prog Ser 157:139–146

    Google Scholar 

  48. Pavia H, Toth G, Åberg P (1999) Trade-offs between phlorotannin production and annual growth in natural populations of the brown seaweed Ascophyllum nodusum. J Ecol 87:761–771

    Google Scholar 

  49. Poll WH van de, Eggert A, Buma AGJ, Breeman AM (2001) Effects of UV-B induced DNA damage and photoinhibition on growth of temperate marine red macrophytes: habitat-related differences in UV-B tolerance. J Phycol 37:30–37

    Google Scholar 

  50. Poll WH van de, Hanelt D, Hoyer K, Buma AGJ, Breeman AM (2002) Ultraviolet-B induced cyclobutane-pyrimidine dimer formation and repair in Arctic marine macrophytes. Photochem Photobiol 76:493–501

    Google Scholar 

  51. Poppe F, Hanelt D, Wiencke C (2002) Changes in ultrastructure, photosynthetic activity and pigments in the Antarctic red alga Palmaria decipiens during acclimation to UV radiation. Bot Mar 45:253–261

    Google Scholar 

  52. Rex M, Harris NRP, von der Gathen P, Lehmann R, Braathen GO, Reimer E, Beck A, Chipperfield MP, Alfier R, Allaart M, O’Connor F, Dier H, Dorokhov V, Fast H, Gil M, Kyrö E, Litynska Z, Mikkelsen IS, Molyneux MG, Nakane H, Notholt J, Rummukainen M, Viatte P, Wenger J (1997) Prolonged stratospheric ozone loss in the 1995–96 Arctic winter. Nature 389:835–838

    Google Scholar 

  53. Rex M, Salawitch RJ, Harris NRP, von der Gathen P, Braathen GO, Schulz A, Deckelmann H, Chipperfield M, Sinnhuber B-M, Reimer E, Alfier R, Bevilacqua R,Hoppel K, Fromm M, Lumpe J, Küllmann H,Kleinböhl A, Bremer H, König M, Künzi K, Toohey D, Vömel H, Richard E, Aikin K, Jost H, Greenblatt JB, Loewenstein M, Podolske JR, Webster CR, Flesch GJ, Scott DC, Herman R, Margitan L, Elkins JW, Ray EA, Moore FL, Hurst DF, Romashkin P, Toon GC, Sen BJJ, Wennberg P, Neuber R, Allart M, Bojkov RB, Claude H, Davies J, Davies W, Backer H, de Dier H, Dorokhov V, Fast, H, Kondo Y, Kyrö E, Litynska Z, Mikkelsen IS, Molyneux MJ, Moran E, Murphy G, Nagai T, Nakane H, Parrondo C, Ravegnani F, Skrivankova P, Viatte P, Yushkov V (2002) Chemical loss of Arctic ozone in winter 1999/2000. J Geophys Res 107, D20, 8276. DOI 10.1029/2001JD000533

  54. Robberecht R, Caldwell MM (1978) Leaf epidermal transmittance of ultraviolet radiation and its implications for plant sensitivity to ultraviolet-radiation induced injury. Oecologia (Berl.) 32:277–287

    Google Scholar 

  55. Roleda MY, Hanelt D, Kräbs G, Wiencke C (2004a) Morphology, growth, photosynthesis and pigments in Laminaria ochroleuca (Laminariales, Phaeophyta) under ultraviolet radiation. Phycologia 43:603–613

    Google Scholar 

  56. Roleda MY, van de Poll WH, Hanelt D, Wiencke C (2004b) PAR and UVBR effects on photosynthesis, viability, growth and DNA in different life stages of two coexisting Gigartinales: implications for recruitment and zonation pattern. Mar Ecol Prog Ser 281:37–50

    Google Scholar 

  57. Roy S (2000) Strategies for the minimisation of UV-induced damage. In: de Mora S, Demers S, Vernet, M (eds) The effects of UV radiation in the marine environment. Cambridge University Press, Cambridge, pp 177–205

    Google Scholar 

  58. Schoenwaelder MEA (2002) The occurrence and cellular significance of physodes in brown algae. Phycologia 41:125–139

    Google Scholar 

  59. Setlow RB (1974) The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. Proc Nat Acad Sci USA 71:3363–3366

    Google Scholar 

  60. Solomon S (1999) Statospheric ozone depletion: a review of concepts and history. Rev Geophys 37:275–316

    Google Scholar 

  61. Stähelin J, Harris NRP, Appenzeller C, Eberhard J (2001) Ozone trends: a review. Rev Geophys 39:231–290

    Google Scholar 

  62. Starr RC, Zeikus JA (1993) UTEX—the culture collection of algae at the University of Texas at Austin. J Phycol 29 (Suppl.):1–106

    Google Scholar 

  63. Steinberg PD (1984) Algal chemical defense against herbivores: allocation of phenolic compounds in the kelp Alaria marginata. Science 223:405–406

    Google Scholar 

  64. Strömgren T, Nielsen MV (1986) Effect of diurnal variations in natural irradiance on the apical length growth and light saturation of growth in five species of benthic macroalgae. Mar Biol (Berl) 90:467–472

    Google Scholar 

  65. Suzuki L, Johnson CH (2001) Algae know the time of day: circadian and photoperiodic programs. J Phycol 37:933–942

    Google Scholar 

  66. Vincent WF, Neale PJ (2000) Mechanisms of UV damage to aquatic organisms. In: de Mora S, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment. Cambridge University Press, Cambridge, pp 149–176

    Google Scholar 

  67. Vink AA, Bergen-Henegouwen JB, Nikaido O, Baan RP, Roza L (1994) Removal of UV-induced DNA lesions in mouse epidermis soon after irradiation. Photochem Photobiol 24:25–31

    Google Scholar 

  68. Wiencke C (1990a) Seasonality of brown macroalgae from Antarctica- a long-term culture study under fluctuating Antarctic daylengths. Polar Biol 10:589–600

    Google Scholar 

  69. Wiencke C (1990b) Seasonality of red and green macroalgae from Antarctica- a long-term culture study under fluctuating Antarctic daylengths. Polar Biol 10:601–607

    Google Scholar 

  70. Wiencke C, Gómez I, Pakker H, Flores-Moya A, Altamirano M, Hanelt D, Bischof K, Figueroa F-L (2000) Impact of UV radiation on viability, photosynthetic characteristics and DNA of brown algal zoospores: implications for depth zonation. Mar Ecol Prog Ser 197:217–229

    Google Scholar 

  71. Wiencke C, Clayton MN, Schoenwaelder M (2004) Sensitivity and acclimation to UV radiation of zoospores from five species of Laminariales from the Arctic. Mar Biol 145:31–39

    Google Scholar 

Download references

Acknowledegments

The first author is supported by a scholarship from the German Academic Exchange Service (DAAD). We thank A. Gruber for collecting field materials and C. Daniel for pigment analysis. This is publication awi-n 14975 of the Alfred Wegener Institute for Polar and Marine Research.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Michael Y. Roleda.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Roleda, M.Y., Hanelt, D. & Wiencke, C. Growth kinetics related to physiological parameters in young Saccorhiza dermatodea and Alaria esculenta sporophytes exposed to UV radiation. Polar Biol 28, 539–549 (2005). https://doi.org/10.1007/s00300-004-0713-2

Download citation

Keywords

  • Photosynthetically Active Radiation
  • Light Phase
  • Brown Macroalgae
  • Young Sporophyte
  • Natural Solar Radiation