, Volume 52, Issue 3, pp 444–455 | Cite as

A sunny day at the beach: Ecophysiological assessment of the photosynthetic adaptability of coastal dune perennial herbs by chlorophyll fluorescence parameters

  • R. Bermúdez
  • R. Retuerto
Original Papers


Light is critical in determining plant structure and functioning in dune ecosystems, which are characterised by high incident and reflected radiation. Light variations demand great plasticity of the photosynthetic apparatus. This study assessed the phenotypic plasticity of foredune species by analysing their light response and dark recovery curves measured under field conditions. We also addressed the question how coexisting species, structurally distinct, differed in their photochemical efficiency in response to short-term changes in light. Finally, we examined how the varying intensity of stressors operating along a dune gradient affected responses to light. The species differed in light use strategies but showed similar patterns of the dark recovery. Species differences in photochemistry varied seasonally, with species being winter specialists, summer specialist or generalists. Some aspects of their photochemistry varied significantly along the gradient. Unexpectedly, other traits did not vary as predicted. For example, changes in light efficiency of plants along the gradient were not consistent with assumed directional changes in the severity of stressors. The different light use strategies observed in coexisting species did not conform to the prediction that stressors constrain the range of possible functional designs in harsh environments. However, the species followed very similar patterns of post-illumination recovery, which suggests that evolutionary pressures might be acting to maintain similar recovery mechanisms. Our results indicated that dune gradients might be nondirectional, which determines unpredictable patterns of variation in leaf traits along the dune gradient. Seasonal differences in the relative performance may allow species to coexist where otherwise one species would exclude the other.

Additional key words

Eryngium maritimum Euphorbia paralias light curve Matthiola sinuata nonphotochemical quenching Pancratium maritimum photochemical quenching quantum yield of photosystem II 



minimal fluorescence of the dark-adapted leaf


minimal fluorescence of the light-adapted leaf


maximal fluorescence of the dark-adapted leaf


maximal fluorescence of the light-adapted leaf


maximum quantum yield of PSII


nonphotochemical quenching index


photochemical quenching index


effective quantum yield of PSII


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  1. Adams III, W.W., Demmig-Adams, B.: Chlorophyll fluorescence as a tool to monitor plant response to the environment. — In: Papageorgiou, G., Govindjee (ed.): Chlorophyll a Fluorescence: Advances in Photosynthesis and Respiration Pp. 583–604. Springer, Dordrecht 2004.CrossRefGoogle Scholar
  2. Andersone, U., Druva-Lusite, I., Ievina, B. et al.: The use of nondestructive methods to assess a physiological status and conservation perspectives of Eryngium maritimum L. — J. Coast Conserv. 15: 509–522, 2011.CrossRefGoogle Scholar
  3. Baker, N.R., Rosenqvist, E.: Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. — J. Exp. Bot. 55: 1607–1621, 2004.CrossRefPubMedGoogle Scholar
  4. Barbour, M.G., DeJong, T.M., Pavlik, B.M.: Marine beach and dune plant communities. — In: Chabot B.F., Mooney H.A. (ed.): Physiological Ecology of North American Plant Communities. Pp. 296–322. Chapman and Hall, New York 1985.CrossRefGoogle Scholar
  5. Battaglia, M.A., Mou, P., Palik, B., Mitchell, R.J.: The effect of spatially variable overstory on the understory light environment of an open-canopied longleaf pine forest. — Can. J. Forest Res. 32: 1984–1991, 2002.CrossRefGoogle Scholar
  6. Bermúdez, R., Retuerto, R.: Living the difference: alternative functional designs in five perennial herbs coexisting in a coastal dune environment. — Funct. Plant Biol. 40: 1187–1198, 2013.CrossRefGoogle Scholar
  7. Bilger, W., Björkman, O.: Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. — Photosynth. Res. 25: 173–185, 1990.CrossRefPubMedGoogle Scholar
  8. Björkman, O., Demmig-Adams, B.: Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. — In: Schulze E.-D., Caldwell M.M. (ed.): Ecophysiology of Photosynthesis. Pp. 17–47. Springer Verlag, Berlin 1995.CrossRefGoogle Scholar
  9. Björkman, O., Demmig, B.: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. — Planta 170: 489–504, 1987.CrossRefPubMedGoogle Scholar
  10. Bucci, S.J., Goldstein, G., Meinzer, F.C. et al.: Functional convergence in hydraulic architecture and water relations of tropical savanna trees: from leaf to whole plant. — Tree Physiol. 24: 891–899, 2004.CrossRefPubMedGoogle Scholar
  11. Buschmann, C.: Photochemical and non-photochemical quenching coefficients of the chlorophyll fluorescence: Comparison of variation and limits. — Photosynthetica 37: 217–224, 1999.CrossRefGoogle Scholar
  12. Butler, W.L.: Tripartite and bipartite models of the photochemical apparatus of photosynthesis. — Ciba Found. Symp. 237–256, 1978.Google Scholar
  13. Cakan, H., Karatas, C.: Interactions between mycorrhizal colonization and plant life forms along the successional gradient of coastal sand dunes in the eastern Mediterranean, Turkey. — Ecol. Res. 21: 301–310, 2006.CrossRefGoogle Scholar
  14. Camprubi, A., Calvet, C., Cabot, P., Pitet, M., Estaun, V.: Arbuscular mycorrhizal fungi associated with psammophilic vegetation in Mediterranean coastal sand dunes. — Span. J. Agric. Res. 8: S96–S102, 2010.CrossRefGoogle Scholar
  15. Camprubi, A., Estaun, V., Calvet, C.: Greenhouse inoculation of psammophilic plant species with arbuscular mycorrhizal fungi to improve survival and early growth. — Eur. J. Soil. Biol. 47: 194–197, 2011.CrossRefGoogle Scholar
  16. Chapman, V.J.: Coastal Vegetation. Pp. 292. Pergamon Press, Oxford 1976.Google Scholar
  17. Ciccarelli, D., Forino, L.M.C., Balestri, M., Pagni, A.: Leaf anatomical adaptations of Calystegia soldanella, Euphorbia paralias and Otanthus maritimus to the ecological conditions of coastal sand dune systems. — Caryologia 62: 142–151, 2009.CrossRefGoogle Scholar
  18. Costa, C.S.B., Cordazzo, C.V., Seeliger, U.: Shore disturbance and dune plant distribution. — J. Coastal Res. 12: 133–140, 1996.Google Scholar
  19. Crawford, R.M.M.: Studies in Plant Survival: Ecological Case Histories of Plant Adaptation to Adversity. Pp. 296. Blackwell Scientific Publications, Oxford 1989.Google Scholar
  20. Crawley, M.J.: The R Book. Pp. 942. John Wiley & Sons Ltd., Chichester 2007.CrossRefGoogle Scholar
  21. Davy, A.J., Figueroa, M.E.: The colonization of strandlines. — In: Miles J., Walton D.W.H. (ed.): Primary Succession on Land. Pp. 113–131. Blackwell Scientific, Boston 1993.Google Scholar
  22. Demmig-Adams, B., Adams, W.W.: Photoprotection and other responses of plants to high light stress. — Annu. Rev. Plant Phys. 43: 599–626, 1992.CrossRefGoogle Scholar
  23. Elhaak, M.A., Migahid, M.M., Wegmann, K.: Ecophysiological studies on Euphorbia paralias under soil salinity and sea water spray treatments. — J. Arid Environ. 35: 459–471, 1997.CrossRefGoogle Scholar
  24. Fitter, A.L., Hay, R.K.M.: Environmental Physiology of Plants. Pp. 367. Academic Press, London 2001.Google Scholar
  25. Fox, J.: car: Companion to Applied Regression. R Package version 1.2–16,, 2009.
  26. Gagné, J.M., Houle, G.: Facilitation of Leymus mollis by Honckenya peploides on coastal dunes in subarctic Quebec, Canada. — Can. J. Bot. 79: 1327–1331, 2001.Google Scholar
  27. Genty, B., Briantais, J.M., Baker, N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. — Biochim. Biophys. Acta 990: 87–92, 1989.CrossRefGoogle Scholar
  28. Gilbert, M.E., Pammenter, N.W., Ripley, B.S.: Could the trade-off between plant burial responses and light-competition result in the zonation of dune vegetation? — S. Afr. J. Bot. 73: 289, 2007.CrossRefGoogle Scholar
  29. Grant, O.M., Tronina, L., Ramalho, J.C. et al.: The impact of drought on leaf physiology of Quercus suber L. trees: comparison of an extreme drought event with chronic rainfall reduction. — J. Exp. Bot. 61: 4361–4371, 2010.CrossRefPubMedGoogle Scholar
  30. Griffiths, M.E.: Salt spray and edaphic factors maintain dwarf stature and community composition in coastal sandplain heathlands. — Plant Ecol. 186: 69–86, 2006.CrossRefGoogle Scholar
  31. Hesp, P.A.: Ecological processes and plant adaptations on coastal dunes. — J. Arid. Environ. 21: 165–191, 1991.Google Scholar
  32. Hodson, M.J., Smith, M.M., Wainwright, S.J., Opik, H.: Cation cotolerance in a salt-tolerant clone of Agrostis stolonifera L. — New Phytol. 90: 253–261, 1982.CrossRefGoogle Scholar
  33. Horton, P., Hague, A.: Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts. IV. Resolution of non-photochemical quenching. — Biochim. Biophys. Acta 932: 107–115, 1988.CrossRefGoogle Scholar
  34. Houle, G.: Interactions between resources and abiotic conditions control plant performance on subarctic coastal dunes. — Am. J. Bot. 84: 1729–1737, 1997a.CrossRefPubMedGoogle Scholar
  35. Houle, G.: No evidence for interspecific interactions between plants in the first stage of succession on coastal dunes in subarctic Quebec, Canada. — Can. J. Bot. 75: 902–915, 1997b.CrossRefGoogle Scholar
  36. Ishikawa, S.I., Furukawa, A., Oikawa, T.: Zonal plant distribution and edaphic and micrometeorological conditions on a coastal sand dune. — Ecol. Res. 10: 259–266, 1995.CrossRefGoogle Scholar
  37. Kachi, N., Hirose, T.: Multivariate approaches of the plant communities related with edaphic factors in the dune system at Azigaura, Ibaraki Pref. I. Association-analysis. — Jpn. J. Ecol. 29: 17–27, 1979.Google Scholar
  38. Kim, D., Yu, K.B.: A conceptual model of coastal dune ecology synthesizing spatial gradients of vegetation, soil, and geomorphology. — Plant Ecol. 202: 135–148, 2009.CrossRefGoogle Scholar
  39. Krause, G.H., Vernotte, C., Briantais, J.M.: Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae. Resolution into two components. — Biochim. Biophys. Acta 679: 116–124, 1982.CrossRefGoogle Scholar
  40. Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis — the basics. — Annu. Rev. Plant Phys. 42: 313–349, 1991.CrossRefGoogle Scholar
  41. Liakopoulos, G., Nikolopoulos, D., Klouvatou, A., Vekkos, K.A., Manetas, Y., Karabourniotis, G.: The photoprotective role of epidermal anthocyanins and surface pubescence in young leaves of grapevine (Vitis vinifera). — Ann. Bot.-London 98: 257–265, 2006.CrossRefGoogle Scholar
  42. Lichtenthaler, H.K., Burkart, S.: Photosynthesis and high light stress. — Bulg. J. Plant Physiol. 25: 3–16, 1999.Google Scholar
  43. Long, S.P., Humphries, S., Falkowski, P.G.: Photoinhibition of photosynthesis in nature. — Annu. Rev. Plant Phys. 45: 633–662, 1994.CrossRefGoogle Scholar
  44. Lortie, C.J., Cushman, J.H.: Effects of a directional abiotic gradient on plant community dynamics and invasion in a coastal dune system. — J. Ecol. 95: 468–481, 2007.CrossRefGoogle Scholar
  45. Maruyama, K., Miura, S.: [Studies on the soil-vegetation system in the west Niigata coastal sand dune, with special reference to the comparison of affected and controlled areas by wind-blown sand.] — Bull. Niigata Univ. For. 14: 43–78, 1981. [In Japanese]Google Scholar
  46. Maun, M.A.: Adaptations enhancing survival and establishment of seedlings on coastal dune systems. — Vegetatio 111: 59–70, 1994.Google Scholar
  47. Maun, M.A.: The Biology of Coastal Sand Dunes. Pp. 265. Oxford University Press, New York 2009.Google Scholar
  48. Maxwell, K., Johnson, G.N.: Chlorophyll fluorescence — a practical guide. — J. Exp. Bot. 51: 659–668, 2000.CrossRefPubMedGoogle Scholar
  49. McLachlan, A., Brown, A.C.: The Ecology of Sandy Shores. Pp. 392. Academic Press 2006.Google Scholar
  50. Meinzer, F.C.: Functional convergence in plant responses to the environment. — Oecologia 134: 1–11, 2003.CrossRefPubMedGoogle Scholar
  51. Miura, S., Maruyama, K.: [Effects of the coastal forest upon soilvegetation system in sand dune. Examples at Kaetsu-District in Niigata prefecture.] — Bull. Niigata Univ. For. 16: 9–36, 1983. [In Japanese]Google Scholar
  52. Mohammad, M.J., Hamad, S.R., Malkawi, H.I.: Population of arbuscular mycorrhizal fungi in semi-arid environment of Jordan as influenced by biotic and abiotic factors. — J. Arid Environ. 53: 409–417, 2003.CrossRefGoogle Scholar
  53. Mohammed, G.H., Binder, W.D., Gillies, S.L.: Chlorophyll fluorescence — A review of its practical forestry applications and instrumentation. — Scand. J. Forest Res. 10: 383–410, 1995.CrossRefGoogle Scholar
  54. Monteith, J.L., Moss, C.J.: Climate and the efficiency of crop production in Britain. — Philos. T. Roy. Soc. B 281: 277–294, 1977.CrossRefGoogle Scholar
  55. Naumann, J.C., Young, D.R., Anderson, J.E.: Spatial variations in salinity stress across a coastal landscape using vegetation indices derived from hyperspectral imagery. — Plant. Ecol. 202: 285–297, 2009.CrossRefGoogle Scholar
  56. Osmond, C.B.: What is photoinhibition? Some insights from comparison of shade and sun plants. — In: Baker N.R., Bowyer J.R. (ed.): Photoinhibition of Photosynthesis from Molecular Mechanisms to the Field. Pp. 1–24. Bios Scientific Publishers, Oxford 1994.Google Scholar
  57. Paruelo, J.M., Jobbagy, E.G., Sala, O.E., Lauenroth, W.K., Burke, I.C.: Functional and structural convergence of temperate grassland and shrubland ecosystems. — Ecol. Appl. 8: 194–206, 1998.CrossRefGoogle Scholar
  58. Payne, A.M., Maun, M.A.: Reproduction and survivorship of Cakile edentula var. lacustris along the lake Huron shoreline. — Am. Midl. Nat. 111: 86–95, 1984.CrossRefGoogle Scholar
  59. Peek, M.S., Russek-Cohen, E., Wait, D.A., Forseth, I.N.: Physiological response curve analysis using nonlinear mixed models. — Oecologia 132: 175–180, 2002.CrossRefGoogle Scholar
  60. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D.: R Core team: nlme: Linear and Nonlinear Mixed Effects Models., 2009
  61. Pospíšil, P.: Mechanisms of non-photochemical chlorophyll fluorescence quenching in higher plants. — Photosynthetica 34: 343–355, 1997.CrossRefGoogle Scholar
  62. Pugnaire, F.I., Haase, P.: Comparative physiology and growth of two perennial tussock grass species in a semi-arid environment. — Ann. Bot. 77: 81–86, 1996.CrossRefGoogle Scholar
  63. Pugnaire, F.I., Haase, P., Incoll, L.D., Clark, S.C.: Response of the tussock grass Stipa tenacissima to watering in a semi-arid environment. — Funct. Ecol. 10: 265–274, 1996.CrossRefGoogle Scholar
  64. R Development Core Team: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna 2011.Google Scholar
  65. Ripley, B.S., Pammenter, N.W., Smith, V.R.: Function of leaf hairs revisited: The hair layer on leaves Arctotheca populifolia reduces photoinhibition, but leads to higher leaf temperatures caused by lower transpiration rates. — J. Plant Physiol. 155: 78–85, 1999.CrossRefGoogle Scholar
  66. Ritchie, R.J.: Fitting light saturation curves measured using modulated fluorometry. — Photosynth. Res. 96: 201–215, 2008.CrossRefPubMedGoogle Scholar
  67. Roháček, K.: Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. — Photosynthetica 40: 13–29, 2002.CrossRefGoogle Scholar
  68. Roháček, K., Soukupová, J., Barták, M.: Chlorophyll fluorescence: A wonderful tool to study plant physiology and plant stress. — In: Schoefs B. (ed.): Plant Cell Compartments — Selected topics. Pp. 41–104. Research Signpost, Kerala 2008.Google Scholar
  69. Ruiz-Sánchez, M., Aroca, R., Muñoz, Y., Polón, R., Ruiz-Lozano, J.M.: The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. — J. Plant Physiol. 167: 862–869, 2010.CrossRefPubMedGoogle Scholar
  70. Salzman, A.G., Parker, M.A.: Neighbors ameliorate local salinity stress for a rhizomatous plant in a heterogeneous environment. — Oecologia 65: 273–277, 1985.CrossRefGoogle Scholar
  71. Skelton, R.P., Midgley, J.J., Nyaga, J.M., Johnson, S.D., Cramer, M.D.: Is leaf pubescence of Cape Proteaceae a xeromorphic or radiation-protective trait? — Aust. J Bot. 60: 104–113, 2012.CrossRefGoogle Scholar
  72. Stoutjesdijk, P.H., Barkman, J.J.: Microclimate, Vegetation and Fauna. Pp. 216. Opulus Press AB, Grangärde1992.Google Scholar
  73. Valladares, F., Wright, S.J., Lasso, E., Kitajima, K., Pearcy, R.W.: Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. — Ecology 81: 1925–1936, 2000.CrossRefGoogle Scholar
  74. Watkinson, A.R., Harper, J.L.: The demography of a sand dune annual: Vulpia fasciculata: I. The natural regulation of populations. — J. Ecol. 66: 15–33, 1978.CrossRefGoogle Scholar
  75. Whatley, M., Whatley, F.R.: Light and Plant Life. Pp. 92. Edward Arnold Limited, London 1980.Google Scholar
  76. Williams, E.L., Hovenden, M.J., Close, D.C.: Strategies of light energy utilisation, dissipation and attenuation in six co-occurring alpine heath species in Tasmania. — Funct. Plant Biol. 30: 1205–1218, 2003.CrossRefGoogle Scholar
  77. Woodward, F.I.: Climate and Plant Distribution. Pp. 174. Cambridge University Press, Cambridge 1987.Google Scholar
  78. Zar, J.H.: Biostatistical Analysis. Pp. 718. Prentice-Hall International, New York 1984Google Scholar

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© The Institute of Experimental Botany 2014

Authors and Affiliations

  1. 1.Department of Biologia Celular y EcologiaUniversity of Santiago de CompostelaSantiago de CompostelaSpain

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