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Marine Biology

, Volume 160, Issue 3, pp 503–517 | Cite as

Influence of local environmental conditions on the seasonal acclimation process and the daily integrated production rates of Laminaria digitata (Phaeophyta) in the English Channel

  • Gaspard DelebecqEmail author
  • Dominique Davoult
  • Dominique Menu
  • Marie-Andrée Janquin
  • Jean-Claude Dauvin
  • François Gevaert
Original Paper

Abstract

Two populations of Laminaria digitata (Hudson) Lamouroux (Ann Mus Hist Nat Paris 20:21–47, 1813) were examined for their seasonal photosynthetic acclimation to clear and turbid-light environments along the French coast of the English Channel. Photosynthesis–irradiance curves, pigment concentrations and the daily in situ integrated oxygen production rates were measured in both populations. Despite the great differences in light attenuation between the sites, the two populations achieved similar oxygen production rates in the field, in relation to high maximal photosynthetic rates, total pigment concentrations and antenna (fucoxanthin + chlorophyll c)/chl a pigment ratios in sporophytes from the turbid environment. Environmental conditions (i.e. light, temperature and nitrogen availability) changed throughout the year in both sites. While the seasonal acclimation trends were evident in the clear-light environment, the strategy in the turbid-light environment differed, tending to maximize light capture throughout the year. This study highlights the diversity of the response of a single species to contrasted light environments.

Keywords

Macroalgae Dissolve Inorganic Nitrogen Light Attenuation Pigment Concentration Oxygen Production 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We would like to thank L. Lévêque, the Service Mer and Observation of the Station Biologique de Roscoff, and also A. Migné for their valuable support during field experiments; T. Cariou from the Station Biologique de Roscoff for providing surface PAR; and the Marel network (Marel Carnot, IFREMER) and the SOMLIT service, managed by Institut National des sciences de l’Univers (INSU), for providing the environmental data. We also thank J. Dekaezemaker for his help in pigment analyses, M. Thorel and V. Delebecq for their assistance in laboratory and field measurements, G. Levavasseur for receiving, helping and supplying the materials and H. Loisel for highly valuable comments on light measurements. We are grateful to the anonymous referees whose suggestions and comments helped strengthen the paper. This study was funded by the Agence Nationale de la Recherche (ANR ECOKELP). We are also grateful to all the ECOKELP team, especially to M. Valero and C. Destombe, for valuable comments on the ecotypic differentiation in macroalgae.

References

  1. Airoldi L, Beck MW (2007) Loss, status and trends for coastal marine habitats of Europe. Oceanogr Mar Biol 45:345–405Google Scholar
  2. Anderson JAM, Chow WS, Park Y-I (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46:129–139CrossRefGoogle Scholar
  3. Anthony KRN, Ridd PV, Orpin AR, Larcombe P, Lough J (2004) Temporal variation of light availability in coastal benthic habitats: effects of clouds, turbidity, and tides. Limnol Oceanogr Annu Rev 45:345–405Google Scholar
  4. Arsalane W, Rousseau B, Duval JC (1994) Influence of the pool size of the xanthophyll cycle on the effect of light stress in a diatom: competition between photoprotection and photoinhibition. Photochem Photobiol 60:237–243CrossRefGoogle Scholar
  5. Aumack CF, Dunton KH, Burd AB, Funk DW, Maffione RA (2007) Linking light attenuation and suspended sediment loading to benthic productivity within an arctic kelp-bed community. J Phycol 43:853–863CrossRefGoogle Scholar
  6. Billot C, Engel CR, Rousvoal S, Kloareg B, Valero M (2003) Current patterns, habitat discontinuities and population genetic structure: the case of the kelp Laminaria digitata in the English Channel. Mar Ecol Progr Ser 253:111–121CrossRefGoogle Scholar
  7. Campbell SJ, Bite JS, Burridge TR (1999) Seasonal patterns in the photosynthetic capacity, tissue pigment and nutrient content of different developmental stages of Undaria pinnatifida (Phaeophyta: Laminariales) in Port Phillip Bay, South-Eastern Australia. Bot Mar 42:231–241CrossRefGoogle Scholar
  8. Coleman MA, Roughan M, Macdonald HS, Connell SD, Gillanders BM, Kelaher B, Steinberg PD (2011) Variation in the strength of continental boundary currents determines continent-wide connectivity in kelp. J Ecol 99:1026–1032CrossRefGoogle Scholar
  9. Cosson J (1999) Sur la disparition progressive de Laminaria digitata sur les côtes du Calvados (France). Cryptog Algol 20:35–42CrossRefGoogle Scholar
  10. Davison IR (1991) Environmental effects on algal photosynthesis: temperature. J Phycol 27:2–8CrossRefGoogle Scholar
  11. Davison IR, Andrews M, Stewart WDP (1984) Regulation of growth in Laminaria digitata: use of in vivo nitrate reductase activities as an indicator of nitrogen limitation in field populations of Laminaria spp. Mar Biol 84:207–217CrossRefGoogle Scholar
  12. Davoult D, Migné A, Spilmont N (2004) Multiscale in situ measurements of intertidal benthic production and respiration. In: Stuntton P, Seuront L (eds) Handbook of scaling methods in aquatic ecology: measurements, analysis and simulation. CRC Press, LLC, New York, pp 97–107Google Scholar
  13. Delebecq G, Davoult D, Menu D, Janquin M-A, Migné A, Dauvin J-C, Gevaert F (2011) In situ photosynthetic performance of Laminaria digitata (Phaeophyceae) during spring tides in Northern Brittany. Cah Biol Mar 52:405–414Google Scholar
  14. Delieu T, Walker DA (1981) Polarographic measurement of photosynthetic exchange evolution by leaf discs. New Phytol 89:165–178CrossRefGoogle Scholar
  15. Demmig-Adams B III, Adams WW (1996) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198:460–470CrossRefGoogle Scholar
  16. Denny MW, Paine RT (1998) Celestial mechanics, sea-level changes, and intertidal ecology. Biol Bull 194:108–115CrossRefGoogle Scholar
  17. Drew EA (1983) Physiology of Laminaria II. Seasonal variation of photosynthesis and respiration in Laminaria digitata Lamour., L. hyperborea (Gunn.) Fosl. and L. saccharina, (L.) Lamour. and a model for calculation of annual carbon budgets. Mar Ecol 4:227–250CrossRefGoogle Scholar
  18. Dring MJ, Lüning K (1994) Influence of spring-neap tidal cycles on the light available for photosynthesis by benthic marine plants. Mar Ecol Progr Ser 104:131–137CrossRefGoogle Scholar
  19. Dunton KH, Jodwalis CM (1988) Photosynthetic performance of Laminaria solidungula measured in situ in the Alaskan High Arctic. Mar Biol 98:277–285CrossRefGoogle Scholar
  20. Eilers PHC, Peeters JCH (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol Model 42:199–215CrossRefGoogle Scholar
  21. Enríquez S, Duarte CM, Sand-Jensen K, Nielsen LS (1996) Broad-scale comparison of photosynthetic rates across phototrophic organisms. Oecologia 108:197–206Google Scholar
  22. Fain SR, Murray SN (1982) Effects of light and temperature on net photosynthesis and dark respiration of gametophytes and embryonic sporophytes of Macrocystis pyrifera. J Phycol 18:92–98CrossRefGoogle Scholar
  23. Fairhead VA, Cheschire AC (2004) Seasonal and depth related variation in the photosynthesis-irradiance response of Ecklonia radiata (Phaeophyta, Laminariales) at West Island, South Australia. Mar Biol 145:415–426Google Scholar
  24. Falkowski PG, Raven JA (1997) Aquatic photosynthesis. Blackwell Scientific Ltd, Oxford 375 pGoogle Scholar
  25. Garcia-Mendoza E, Colombo-Pallotta MF (2007) The giant kelp Macrocystis pyrifera presents a different nonphotochemical quenching control than higher plants. New Phytol 173:526–536CrossRefGoogle Scholar
  26. Gerard VA (1988) Ecotypic differentiation in light-related traits of the kelp Laminaria saccharina. Mar Biol 97:25–36CrossRefGoogle Scholar
  27. Gerard VA, Du Bois KR (1988) Temperature ecotypes near the southern boundary of the kelp Laminaria saccharina. Mar Biol 97:575–580CrossRefGoogle Scholar
  28. Gevaert F, Creach A, Davoult D, Holl A-C, Seuront L, Lemoine Y (2002) Photo-inhibition and seasonal photosynthetic performance of the seaweed Laminaria saccharina during a simulated tidal cycle: chlorophyll fluorescence measurements and pigment analysis. Plant Cell Environ 25:859–872CrossRefGoogle Scholar
  29. Gevaert F, Créach A, Davoult D, Migné A, Levavasseur G, Arzel P, Holl A-C, Lemoine Y (2003) Laminaria saccharina photosynthesis measured in situ: photoinhibition and xanthophyll cycle during a tidal cycle. Mar Ecol Progr Ser 247:43–50CrossRefGoogle Scholar
  30. Gevaert F, Janquin M-A, Davoult D (2008) Biometrics in Laminaria digitata: a useful tool to assess biomass, carbon and nitrogen contents. J Sea Res 60:215–219CrossRefGoogle Scholar
  31. Gevaert F, Delebecq G, Menu D, Brutier L (2011) A fully automated system for measurements of photosynthetic oxygen exchange under immersed conditions: an example of its use in Laminaria digitata (Heterokontophyta: Phaeophyceae). Limnol Oceanogr Meth 9:361–379CrossRefGoogle Scholar
  32. Gómez I, Wiencke C (1998) Seasonal changes in C, N and major organic compounds and their significance to morpho-functional processes in the endemic Antarctic brown alga Ascoseira mirabilis. Polar Biol 19:115–124CrossRefGoogle Scholar
  33. Hanelt D, Huppertz K, Nultsch W (1993) Daily course of photosynthesis and photoinhibition in marine macroalgae investigated in the laboratory and field. Mar Ecol Progr Ser 97:31–37CrossRefGoogle Scholar
  34. Havaux M, Tardy F (1996) Temperature-dependent adjustment of the thermal stability of the photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. Planta 198:324–333CrossRefGoogle Scholar
  35. Helmuth B, Harley CDG, Halpin P, O’Donnell M, Hofmann GE, Blanchette C (2002) Climate change and latitudinal patterns of intertidal thermal stress. Science 298:1015–1017CrossRefGoogle Scholar
  36. Henley WJ (1993) Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J Phycol 29:729–739CrossRefGoogle Scholar
  37. King RJ, Schramm W (1976) Photosynthetic rates of benthic marine algae in relation to light intensity and seasonal variations. Mar Biol 37:215–222CrossRefGoogle Scholar
  38. Kirk JTO (1994) Light and photosynthesis in aquatic ecosystems, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  39. Küppers U, Weidner M (1980) Seasonal variation of enzyme activities in Laminaria hyperborea. Planta 148:222–230CrossRefGoogle Scholar
  40. Lamouroux JVF (1813) Essai sur les genres de la famille des thalassiophytes non articulées. Ann Mus Hist Nat Paris 20:21–47 115–139, 267–293, pls 7–13Google Scholar
  41. Lavaud J, Rousseau B, van Gorkom HJ, Etienne A-L (2002) Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol 129:1398–1406CrossRefGoogle Scholar
  42. Lavaud J, Strzepek RF, Kroth PG (2007) Photoprotection capacity differs among diatoms: possible consequences in the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnol Oceanogr 52:1188–1194CrossRefGoogle Scholar
  43. Lawson SE, Wiberg PL, McGlathery KJ, Fugate DC (2007) Wind-driven sediment suspension controls light availability in shallow coastal lagoon. Estuar Coast 30:102–112Google Scholar
  44. Lewey SA, Gorham J (1984) Pigment composition and photosynthesis in Sargassum muticum. Mar Biol 80:109–115CrossRefGoogle Scholar
  45. Littler MM, Murray SN, Arnold KE (1979) Seasonal variations in net photosynthetic performance and cover of intertidal macrophytes. Aquat Bot 7:35–46CrossRefGoogle Scholar
  46. Logan BA, Grace SC, Adams WW III, Demmig-Adams B (1998) Seasonal differences in xanthophyll cycle characteristics and antioxidants in Mahonia repens growing in different light environments. Oecologia 116:9–17Google Scholar
  47. Lüning K (1979) Growth strategies of three Laminaria species (Phaeophyceae) inhabiting different depth zones in the sublittoral region of Helgoland (North Sea). Mar Ecol Progr Ser 1:195–207CrossRefGoogle Scholar
  48. Machalek KM, Davison IR, Falkowski PG (1996) Thermal acclimation and photoacclimation of photosynthesis in the brown alga Laminaria saccharina. Plant Cell Environ 19:1005–1016CrossRefGoogle Scholar
  49. Markager S (1993) Light absorption and quantum yield for growth of five species of marine macroalgae. J Phycol 29:54–63CrossRefGoogle Scholar
  50. Markager S, Sand-Jensen K (1992) Light requirements and depth zonation of marine macroalgae. Mar Ecol Progr Ser 88:83–92CrossRefGoogle Scholar
  51. Miller SM, Wing SR, Hurd CL (2006) Photoacclimation of Ecklonia radiata (Laminariales, Heterokontophyta) in Doubtful Sound, Fjordland, Southern New Zealand. Phycologia 45:44–52CrossRefGoogle Scholar
  52. Mislan KAS, Wethey DS, Helmuth B (2009) When to worry about the weather: role of tidal cycle in determining patterns of risk in intertidal ecosystems. Global Change Biol 15:3056–3065CrossRefGoogle Scholar
  53. Moleenar FJ, Breeman AM (1997) Latitudinal trends in the growth and reproductive seasonality of Delesseria sanguinea, Membranoptera alata and Phycodris rubens (Rhodophyta). J Phycol 33:330–343CrossRefGoogle Scholar
  54. Ramus J, Beale SI, Mauzerall D (1976) Correlation of changes in pigment content with photosynthetic capacity of seaweeds as a function of water depth. Mar Biol 37:231–238CrossRefGoogle Scholar
  55. Raven JA (1984) A cost-benefit analysis of photon absorption by photosynthetic unicells. New Phytol 98:593–625CrossRefGoogle Scholar
  56. Raven JA, Geider RJ (2003) Adaptation, acclimation and regulation in algal photosynthesis. In: Larkum WD, Douglas SE, Raven JA (eds) Photosynthesis in Algae, vol 14. Kluwer Academic Publishers, Dordrecht, pp 385–412CrossRefGoogle Scholar
  57. Rodrigues MA, Dos Santos CP, Yoneshigue-Valentin Y, Strbac D, Hall DO (2000) Photosynthetic light-response curves and photoinhibition of the deep-water Laminaria abyssalis and the intertidal Laminaria digitata (Phaeophyceae). J Phycol 36:97–106CrossRefGoogle Scholar
  58. Rohde S, Hiebenthal C, Wahl M, Karez R, Bischof K (2008) Decreased depth distribution of Fucus vesiculosus (Phaeophyceae) in the Western Baltic: effects of light deficiency and epibionts on growth and photosynthesis. Eur J Phycol 43:143–150Google Scholar
  59. Sakanishi Y, Yokohama Y, Aruga Y (1988) Photosynthesis measurement of blade segments of brown algae Ecklonia cava Kjellman and Eisenia bicyclis Setchell. Jpn J Phycol 36:24–28Google Scholar
  60. Sand-Jensen K (1988) Photosynthetic responses of Ulva lactuca at very low light. Mar Ecol Progr Ser 50:195–201CrossRefGoogle Scholar
  61. Serisawa Y, Akino H, Matsuyama K, Ohno M, Tanaka J, Yokohama Y (2002) Morphometric study of Ecklonia cava (Laminariales, Phaeophyta) sporophytes in two localities with different temperature conditions. Phycol Res 50:193–199CrossRefGoogle Scholar
  62. Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences. McGraw-Hill International Editors, New YorkGoogle Scholar
  63. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. W.H. Freeman and Company, San FranciscoGoogle Scholar
  64. Sournia A, Birrien JL, Douvillé JL, Klein B, Viollier M (1987) A daily study of the diatom spring bloom at Roscoff (France) in 1985. I. The spring bloom within the annual cycle. Estuar Coast Shelf Sci 25:355–367CrossRefGoogle Scholar
  65. Spilmont N, Denis L, Artigas LF, Caloin F, Courcot L, Créach A, Desroy N, Gevaert F, Hacquebart P, Hubas C, Janquin M-A, Lemoine Y, Luczak C, Migné A, Rauch M, Davoult D (2009) Impact of the Phaeocystis globosa spring bloom on the intertidal benthic compartment in the eastern English Channel: a synthesis. Mar Pollut Bull 58:55–63CrossRefGoogle Scholar
  66. Staehr PA, Wernberg T (2009) Physiological responses of Ecklonia radiata (laminariales) to a latitudinal gradient in ocean temperature. J Phycol 45:91–99CrossRefGoogle Scholar
  67. Stengel DB, Dring MJ (1998) Seasonal variation in the pigment content and photosynthesis of different thallus regions of Ascophyllum nodosum (Fucales, Phaeophyta) in relation to position in the canopy. Phycologia 37:259–268CrossRefGoogle Scholar
  68. Sukenik A, Bennett J, Falkowski PG (1987) Light-saturated photosynthesis—Limitation by electron transport of carbon fixation? Biochim Biophys Acta 891:205–215CrossRefGoogle Scholar
  69. Terblanche JS, Kleynhans E (2009) Phenotypic plasticity of desiccation resistance in Glossina puparia: are there ecotype constraints on acclimation responses? J Evol Biol 22:1636–1648CrossRefGoogle Scholar
  70. Vantrepotte V, Brunet C, Mériaux X, Lécuyer E, Vellucci V, Santer R (2007) Bio-optical properties of coastal waters in the Eastern English Channel. Estuar Coast Shelf Sci 72:201–212CrossRefGoogle Scholar
  71. Visser MP (1970) The turbidity of the Southern North Sea. Dtsch Hydrogr Z 23:97–117CrossRefGoogle Scholar
  72. Vogt H, Schramm W (1991) Conspicuous decline of Fucus in Kiel Bay (Western Baltic): what are the causes? Mar Ecol Progr Ser 69:189–194CrossRefGoogle Scholar
  73. Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447CrossRefGoogle Scholar
  74. Zheng G, Tian B, Fujuan Z, Tao F, Li W (2011) Plant adaptation to frequent alteration between high and low temperatures: remodeling of membrane lipids and maintenance of unsaturation levels. Plant Cell Environ 34:1431–1442CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Gaspard Delebecq
    • 1
    • 2
    Email author
  • Dominique Davoult
    • 3
    • 4
  • Dominique Menu
    • 2
  • Marie-Andrée Janquin
    • 1
    • 2
  • Jean-Claude Dauvin
    • 5
    • 6
  • François Gevaert
    • 1
    • 2
  1. 1.Université Lille1, Univ Lille Nord de FranceWimereuxFrance
  2. 2.CNRS, UMR 8187 LOGWimereuxFrance
  3. 3.UPMC Univ Paris 06RoscoffFrance
  4. 4.CNRS, UMR 7144 AD2 MRoscoffFrance
  5. 5.Université de Caen Basse NormandieCaenFrance
  6. 6.CNRS, UMR 6143 M2CCaenFrance

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