Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-20T06:36:20.190Z Has data issue: false hasContentIssue false
  • English
  • Français

Adjustment of photoprotection to tidal conditions in intertidal seagrasses

Published online by Cambridge University Press:  30 August 2016

D. Kohlmeier ,
C.A. Pilditch ,
J. F. Bornman  and
K. Bischof
D. Kohlmeier*
Affiliation:
Department of Marine Botany, Faculty Biology/Chemistry, University of Bremen, 28359 Bremen, Germany
C.A. Pilditch
Affiliation:
Department of Biological Sciences, University of Waikato, Private Bag 3105, Hamilton, New Zealand
J. F. Bornman
Affiliation:
International Institute of Agri-Food Security, Curtin University, Perth, Australia
K. Bischof
Affiliation:
Department of Marine Botany, Faculty Biology/Chemistry, University of Bremen, 28359 Bremen, Germany
*
Correspondence should be addressed to: D. Kohlmeier, Department of Marine Botany, Faculty Biology/Chemistry, University of Bremen, 28359 Bremen, Germany email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Light adaptive strategies were studied in a comparative analysis of the congeneric seagrass species Zostera muelleri and Zostera marina at two case study areas in New Zealand and Germany. Surveys in intertidal seagrass meadows were conducted from pre-dawn until sunset on days when either low or high tide coincided with noon. The results show marked fluctuations of photophysiology (optimum and effective quantum yield, non-photochemical quenching, cycling of xanthophyll cycle (XC) pigments) over daily and tidal cycles. At both locations, we observed a near complete conversion (de-epoxidation) of violaxanthin to zeaxanthin at times with high irradiance and a rapid and complete re-epoxidation under subsequent lower light conditions. At the New Zealand site we also observed significantly larger XC-pigment pool sizes in seagrass leaves sampled in a week when low tide coincided with noon (larger daily fluence and higher maximum irradiance), compared with leaves sampled in a week when high tide was at noon. This dynamic adjustment of xanthophyll pool size has not been previously reported for intertidal seagrasses. It adds to our understanding of an important adaptive feature in a highly dynamic light environment and to the general ecology and adaptability of seagrasses.

Keywords

seagrassphotoprotectionxanthophyll cycleintertidal habitatZosteratemperate
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 97 , Special Issue 3: European Marine Biology Symposium , May 2017 , pp. 571 - 579
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ambarsari, I., Brown, B.E., Barlow, R.G., Britton, G. and Cummings, D. (1997) Fluctuations in algal chlorophyll and carotenoid pigments during solar bleaching in the coral Goniastrea aspera at Phuket, Thailand. Marine Ecology Progress Series 159, 303–307.CrossRefGoogle Scholar
Bilger, W. and Björkman, O. (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis . Photosynthesis Research 25, 173–185.CrossRefGoogle ScholarPubMed
Bischof, K., Kräbs, G., Wiencke, C. and Hanelt, D. (2002) Solar ultraviolet radiation affects the activity of ribulose-1,5-bisphosphate carboxylase-oxygenase and the composition of photosynthetic and xanthophyll cycle pigments in the intertidal green alga Ulva lactuca . Planta 215, 502–509.CrossRefGoogle ScholarPubMed
Björk, M., Uku, J., Weil, A. and Beer, S. (1999) Photosynthetic tolerances to desiccation of tropical intertidal seagrasses. Marine Ecology Progress Series 191, 121–126.CrossRefGoogle Scholar
Björkman, O. and Demmig-Adams, B. (1994) Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. In Caldwell, M.M. and Schulze, E.-D. (eds) Ecophysiology of photosynthesis. Berlin: Springer, pp. 17–47.Google Scholar
Brown, B.E., Ambarsari, I, Warner, M.E., Fitt, W.K., Dunne, R.P., Gibb, S.W. and Cummings, D.G. (1999) Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18, 99–105.Google Scholar
Collier, C., Lavery, P., Ralph, P. and Masini, R. (2008) Physiological characteristics of the seagrass Posidonia sinuosa along a depth-related gradient of light availability. Marine Ecology Progress Series 353, 65–79.CrossRefGoogle Scholar
Dawson, S.P. and Dennison, W.C. (1996) Effects of ultraviolet and photosynthetically active radiation on five seagrass species. Marine Biology 125, 629–638.CrossRefGoogle Scholar
Demmig-Adams, B. (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1020, 1–24.CrossRefGoogle Scholar
Demmig-Adams, B. (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant and Cell Physiology 39, 474–482.CrossRefGoogle Scholar
Demmig-Adams, B. and Adams, W.W. (1992) Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology 43, 599–626.CrossRefGoogle Scholar
Ensminger, I., Xyländer, M., Hagen, C. and Braune, W. (2001) Strategies providing success in a variable habitat: III. Dynamic control of photosynthesis in Cladophora glomerata . Plant, Cell and Environment 24, 769–779.CrossRefGoogle Scholar
Eskling, M. and Åkerlund, H.-E. (1998) Changes in the quantities of violaxanthin de-epoxidase, xanthophylls and ascorbate in spinach upon shift from low to high light. Photosynthesis Research 57, 41–50.CrossRefGoogle Scholar
Flanigan, Y.S. and Critchley, C. (1996) Light response of D1 turnover and photosystem II efficiency in the seagrass Zostera capricorni . Planta 198, 319–323.CrossRefGoogle Scholar
Fourqurean, J., Duarte, C.M., Kennedy, H., Marbà, N., Holmer, M., Mateo, M.A., Apostolaki, E.T., Kendrick, G.A., Krause-Jensen, D., McGlathery, K.J. and Serrano, O. (2012) Seagrass ecosystems as a globally significant carbon stock. Nature Geoscience 5, 505–509.CrossRefGoogle Scholar
Franklin, L., Osmond, C.B. and Larkum, A.D. (2003) Photoinhibition, UV-B and algal photosynthesis. In Larkum, A.D., Douglas, S. and Raven, J. (eds) Photosynthesis in algae, Volume 14. Dordrecht: Springer, pp. 351–384.CrossRefGoogle Scholar
García-Plazaola, J.I., Hernández, A., Errasti, E. and Becerril, J.M. (2002) Occurrence and operation of the lutein epoxide cycle in Quercus species. Functional Plant Biology 29, 1075–1080.CrossRefGoogle ScholarPubMed
García-Sánchez, M., Korbee, N., Pérez-Ruzafa, I.M., Marcos, C., Domínguez, B., Figueroa, F.L. and Pérez-Ruzafa, Á. (2012) Physiological response and photoacclimation capacity of Caulerpa prolifera (Forsskål) J.V. Lamouroux and Cymodocea nodosa (Ucria) Ascherson meadows in the Mar Menor lagoon (SE Spain). Marine Environmental Research 79, 37–47.CrossRefGoogle ScholarPubMed
Goss, R. and Jakob, T. (2010) Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynthesis Research 106, 103–122.CrossRefGoogle ScholarPubMed
Hanelt, D., Li, J. and Nultsch, W. (1994) Tidal dependence of photoinhibition of photosynthesis in marine macrophytes of the South China Sea. Botanica Acta 107, 66–72.CrossRefGoogle Scholar
Hily, C., van Katwijk, M.M. and den Hartog, C. (2003) The seagrasses of Western Europe. In Green, E.P. and Short, F.T. (eds) World atlas of seagrasses: present status and future conservation. Berkeley, CA: University of California Press, pp. 38–47.Google Scholar
Hughes, A.R., Stachowicz, J. and Williams, S. (2009) Morphological and physiological variation among seagrass (Zostera marina) genotypes. Oecologia 159, 725–733.CrossRefGoogle ScholarPubMed
Huppertz, K., Hanelt, D. and Nultsch, W. (1990) Photoinhibition of photosynthesis in the marine brown alga Fucus serratus as studied in field experiments. Marine Ecology Progress Series 66, 175–182.CrossRefGoogle Scholar
Inglis, G.J. (2003) Seagrasses of New Zealand. In Green, E.P. and Short, F.T. (eds) World atlas of seagrasses: present status and future conservation. Berkeley, CA: University of California Press, pp. 148–157.Google Scholar
Jahns, P. and Holzwarth, A.R. (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1817, 182–193.CrossRefGoogle ScholarPubMed
Kohlmeier, D., Pilditch, C.A., Bornman, J.F. and Bischof, K. (2014) Site specific differences in morphometry and photophysiology in intertidal Zostera muelleri meadows. Aquatic Botany 116, 104–109.CrossRefGoogle Scholar
Königer, M., Harris, G., Virgo, A. and Winter, K. (1995) Xanthophyll-cycle pigments and photosynthetic capacity in tropical forest species: a comparative field study on canopy, gap and understory plants. Oecologia 104, 280–290.CrossRefGoogle Scholar
Kono, M. and Terashima, I. (2014) Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. Journal of Photochemistry and Photobiology B: Biology 137, 89–99.CrossRefGoogle ScholarPubMed
Lavaud, J., Rousseau, B., van Gorkom, H.J. and Etienne, A.-L. (2002) Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum . Plant Physiology 129, 1398–1406.CrossRefGoogle ScholarPubMed
Leuschner, C. and Rees, U. (1993) CO2 gas exchange of two intertidal seagrass species, Zostera marina L. and Zostera noltii Hornem., during emersion. Aquatic Botany 45, 53–62.CrossRefGoogle Scholar
Marín-Guirao, L., Ruiz, J.M., Sandoval-Gil, J.M., Bernardeau-Esteller, J., Stinco, C.M. and Meléndez-Martínez, A. (2013) Xanthophyll cycle-related photoprotective mechanism in the Mediterranean seagrasses Posidonia oceanica and Cymodocea nodosa under normal and stressful hypersaline conditions. Aquatic Botany 109, 14–24.CrossRefGoogle Scholar
Matheson, F.E., Lundquist, C.J., Gemmill, C.E.C. and Pilditch, C.A. (2011) New Zealand seagrass – more threatened than IUCN review indicates. Biological Conservation 144, 2749–2750.CrossRefGoogle Scholar
Matsubara, S., Krause, G.H., Aranda, J., Virgo, A., Beisel, K.G., Jahns, P. and Winter, K. (2009) Sun-shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants. Functional Plant Biology 36, 20–36.CrossRefGoogle ScholarPubMed
Moore, K. and Short, F. (2006) Zostera: biology, ecology, and management. In Larkum, A., Orth, R.J. and Duarte, C. (eds) Seagrasses: biology, ecology and conservation. Dordrecht: Springer, pp. 361–386.Google Scholar
Ondiviela, B., Losada, I.J., Lara, J. L., Maza, M., Galván, C., Bouma, T. J. and van Belzen, J. (2014) The role of seagrasses in coastal protection in a changing climate. Coastal Engineering 87, 158–168.CrossRefGoogle Scholar
Ralph, P.J., Polk, S.M., Moore, K.A., Orth, R.J. and Smith, W.O. Jr (2002) Operation of the xanthophyll cycle in the seagrass Zostera marina in response to variable irradiance. Journal of Experimental Marine Biology and Ecology 271, 189–207.CrossRefGoogle Scholar
Reise, K. (1985) The tidal flats of Königshafen. In Billings, W.D., Golley, F., Lange, O.L., Olson, H. and Remmert, J.S. (eds) Tidal Flat Ecology, Volume 54. Berlin: Springer, pp. 35–53.CrossRefGoogle Scholar
Schubert, H., Sagert, S. and Forster, R.M. (2001) Evaluation of the different levels of variability in the underwater light field of a shallow estuary. Helgoland Marine Research 55, 12–22.CrossRefGoogle Scholar
Schumacher, J., Dolch, T. and Reise, K. (2014) Transitions in sandflat biota since the 1930s: effects of sea-level rise, eutrophication and biological globalization in the tidal bay Königshafen, northern Wadden Sea. Helgoland Marine Research 68, 289–298.CrossRefGoogle Scholar
Schwarz, A.M. (2004) Contribution of photosynthetic gains during tidal emersion to production of Zostera capricorni in a North Island, New Zealand estuary. New Zealand Journal of Marine and Freshwater Research 38, 809–818.CrossRefGoogle Scholar
Schwarz, A.M., Björk, M., Buluda, T., Mtolera, M. and Beer, S. (2000) Photosynthetic utilisation of carbon and light by two tropical seagrass species as measured in situ . Marine Biology 137(5–6), 755–761.CrossRefGoogle Scholar
Serodio, J. and Catarino, F. (1999) Fortnightly light and temperature variability in estuarine intertidal sediments and implications for microphytobenthos primary productivity. Aquatic Ecology 33, 235–241.CrossRefGoogle Scholar
Short, F.T., Polidoro, B., Livingstone, S.R., Carpenter, K.E., Bandeira, S., Bujang, J.S., Calumpong, H.P., Carruthers, T.J.B., Coles, R.G., Dennison, W.C., Erftemeijer, P.L.A., Fortes, M.D., Freeman, A.S., Jagtap, T.G., Kamal, A.H.M., Kendrick, G.A., Kenworthy, W.J., La Nafie, Y.A., Nasution, I.M., Orth, R.J., Prathep, A., Sanciangco, J.C., van Tussenbroek, B., Vergara, S.G., Waycott, M. and Zieman, J.C. (2011) Extinction risk assessment of the world's seagrass species. Biological Conservation 144, 1961–1971.CrossRefGoogle Scholar
Silva, J., Barrote, I., Costa, M.M., Albano, S. and Santos, R. (2013) Physiological responses of Zostera marina and Cymodocea nodosa to light-limitation stress. PLoS ONE 8, e81058.CrossRefGoogle ScholarPubMed
Silva, J. and Santos, R. (2003) Daily variation patterns in seagrass photosynthesis along a vertical gradient. Marine Ecology Progress Series 257, 37–44.CrossRefGoogle Scholar
Stamenković, M., Bischof, K. and Hanelt, D. (2014) Xanthophyll cycle pool size and composition in several Cosmarium strains (Zygnematophyceae, Streptophyta) are related to their geographic distribution patterns. Protist 165, 14–30.CrossRefGoogle ScholarPubMed
Thayer, S. and Björkman, O. (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynthesis Research 23, 331–343.CrossRefGoogle Scholar
Uhrmacher, S., Hanelt, D. and Nultsch, W. (1995) Zeaxanthin content and the degree of photoinhibition are linearly correlated in the brown alga Dictyota dichotoma . Marine Biology 123, 159–165.CrossRefGoogle Scholar
Vermaat, J.E. (1997) The capacity of seagrasses to survive increased turbidity and siltation: the significance of growth form and light use. Ambio 26, 499–504.Google Scholar
Waycott, M., Duarte, C.M., Carruthers, T.J.B., Orth, R.J., Dennison, W.C., Olyarnik, S., Calladine, A., Fourqurean, J.W., Heck, Jr K.L., Randall Hughes, A., Kendrick, G.A., Kenworthy, W.J., Short, F.T. and Williams, S.L. (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences USA 106, 12377–12381.CrossRefGoogle ScholarPubMed
Wing, S.R. and Patterson, M.R. (1993) Effects of wave-induced lightflecks in the intertidal zone on photosynthesis in the macroalgae Postelsia palmaeformis and Hedophyllum sessile (Phaeophyceae). Marine Biology 116, 519–525.CrossRefGoogle Scholar
Wright, S.W., Jeffrey, S.W., Mantoura, R.F.C., Llewellyn, C.A., Bjørnland, T., Repeta, D. and Welschmeyer, N. (1991) Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Marine Ecology Progress Series 77, 183–196.CrossRefGoogle Scholar
Yamamoto, H.Y., Nakayama, T.O.M. and Chichester, C.O. (1962) Studies on the light and dark interconversions of leaf xanthophylls. Archives of Biochemistry and Biophysics 97, 168–173.CrossRefGoogle ScholarPubMed