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Discrimination between12C and13C by marine plants

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The natural abundance13C/12C ratios (as δ13C) of organic matter of marine macroalgae from Fife and Angus (East Scotland) were measured for comparison with the species' ability to use CO2 and HCO -3 for photosynthesis, as deduced from previously published pH-drift measurements. There was a clear difference in δ13C values for species able or unable to use HCO -3 . Six species of Chlorophyta, 12 species of Phaeophyta and 8 species of Rhodophyta that the pH-drift data suggested could use HCO -3 had δ13C values in the range -8.81‰ to -22.55‰. A further 6 species of Rhodophyta which the pH-drift data suggested could only use CO2 had δ13C values in the range -29.90‰ to-34.51‰. One of these six species (Lomentaria articulata) is intertidal; the other five are subtidal and so have no access to atmospheric CO2 to complicate the analysis. For these species, calculations based on the measured δ13C of the algae, the δ13C of CO2 in seawater, and the known13C/12C discrimination of CO2 diffusion and RUBISCO carboxylation suggest that only 15–21% of the limitation to photosynthesisin situ results from CO2 diffusion from the bulk medium to the plastids; the remaining 79–85% is associated with carboxylation reactions (and, via feedback effects, down-stream processes). This analysis has been extended for one of these five species,Delesseria sanguinea, by incorporating data onin situ specific growth rates, respiratory rates measured in the laboratory, and applying Fick's law of diffusion to calculate a boundary layer thickness of 17–24 μm. This value is reasonable for aDelesseria sanguinea frondin situ. For HCO -3 -using marine macroalgae the range of δ13C values measured can be accommodated by a CO2 efflux from algal cells which range from 0.306 of the gross HCO -3 influx forEnteromorpha intestinalis13C=-8.81‰) in a rockpool to 0.787 forChondrus crispus13C=-22.55‰). The relatively high computed CO2 efflux for those HCO -3 -users with the more negative δ13C values implies a relatively high photon cost of C assimilation; the observed photon costs can be accommodated by assuming coupled, energy-independent inorganic carbon influx and efflux. The observed δ13C values are also interpreted in terms of water movement regimes and obtaining CO2 from the atmosphere. Published δ13C values for freshwater macrophytes were compared with the ability of the species to use CO2 and HCO -3 and again there was an apparent separation in δ13C values for these two groups. δ13C values obtained for marine macroalgae for which no pH-drift data are available permit predictions, as yet untested, as to whether they use predominantly CO2 or HCO -3

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References

  • Allen ED, Spence DHN (1981) The differential ability of aquatic plants to utilize the inorganic carbon supply in freshwaters. New Phytol 87: 269–283

    CAS  Google Scholar 

  • Beardall J (1991) Effects of photon flux density on the “CO2-concentrating mechanism” of the cyanobacteriumAnabaena variabilis. J Plankt Res 13(Suppl): 133–141

    Google Scholar 

  • Beer S, Eshel A (1983) Photosynthesis ofUlva sp. II. Utilization of CO2 and HCO -3 when submerged. J Exp Mar Biol Ecol 70: 99–106

    CAS  Google Scholar 

  • Benson BB, Krause D Jr. (1984) The concentration and isotopic fractionation of oxygen dissolved in freshwater and seawater in equilibrium with the atmosphere. Limnol Oceanogr 29: 620–632

    CAS  Google Scholar 

  • Cooper LW, De Niro MJ (1989) Stable carbon isotope variability in the seagrassPosidonia oceanica: evidence for light intensity effects. Mar Ecol Progr Ser 50: 225–229

    CAS  Google Scholar 

  • Dauby P (1989) The stable carbon isotope ratios in benthic food webs of the Gulf of Calvi, Corsica. Cont Shelf Res 9: 181–195

    Article  Google Scholar 

  • Descolas-Gros C, Fontugne M (1990) Stable carbon isotope fractionation by marine phytoplankton during photosynthesis. Plant Cell Environ 13: 207–218

    CAS  Google Scholar 

  • Ehleringer JR (1991)13C/12C fractionation and its utility in terrestrial plant studies. In: Coleman DC, Fry B (eds), Carbon Isotope Techniques, Academic Press, San Diego, pp 187–200

    Google Scholar 

  • Farquhar GD (1983) On the nature of carbon isotope discrimination in C4 species. Aust J Plant Physiol 10: 205–236

    CAS  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40: 503–537

    Article  CAS  Google Scholar 

  • Fenton GE, Ritz DA (1989) Spatial variability of13C:12C and D:H inEcklonia radiata (C. Ag.), J. Agardh. (Laminariales). Estuarine Coastal Shelf Sci 28:95–101

    CAS  Google Scholar 

  • Fry B, Sherr EB (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib Mar Sci 27: 13–47

    CAS  Google Scholar 

  • Fry B, Lutes R, Notham M, Parker PL, Ogden J (1982) A13C/12C comparison of food webs in Caribbean seagrass meadows and coral reefs. Aquat Bot 15: 389–398

    Google Scholar 

  • Giordano M, Maberly SC (1989) Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81: 534–539

    Article  Google Scholar 

  • Henderson SA, Caemmerer S von, Farquhar GD (1992) Short-term measurements of carbon isotope discrimination in several C4 species. Aust J Plant Physiol 19: 263–285

    CAS  Google Scholar 

  • Goyet C, Poisson A (1989) New determination of carbonic acid dissociation constants in seawater as a function of temperature and salinity. Deep Sea Res 36: 1635–1654

    CAS  Google Scholar 

  • Johnston AM, Maberly SC, Raven JA (1992) The acquisition of inorganic carbon by four red macroalgae from different habitats. Oecologia (in press)

  • Kerby NW, Raven JA (1985) Transport and fixation of inorganic carbon by marine macroalgae. Adv Bot Res 11: 71–123

    CAS  Google Scholar 

  • Kain JM (1984) Seasonal growth of two subtidal species of Rhodophyta off the Isle of Man. J Exp Mar Biol Ecol 82: 207–220

    Google Scholar 

  • Levavesseur G, Edwards GE, Osmond CB, Ramus J (1991) Inorganic carbon limitation of photosynthesis inUlva rotundata (Chlorophyta). J Phycol 27: 667–672

    Google Scholar 

  • Lüning K, Dring MJ (1985) Action spectra and spectral quantum yield of photosynthesis in marine macroalgae with thin and thick thalli. Mar Biol 87: 111–129

    Article  Google Scholar 

  • Lüning K, Schmitz K (1988) Dark growth of the red algaDelesseria sanguinea (Ceramiales): lack of chlorophyll, photosynthetic capacity and phycobilisomes. Phycologia 27: 72–77

    Google Scholar 

  • Maberly SC (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J Phycol 26: 439–449

    Article  CAS  Google Scholar 

  • Maberly SC (1992) Carbonate ions appear to neither inhibit nor stimulate use of bicarbonate ions in photosynthesis byUlva lactuca. Plant Cell Environ 15: 255–260

    CAS  Google Scholar 

  • Macfarlane JJ, Raven JA (1985) External and internal transport inLemanea: Interactions with the kinetics of ribulose bisphosphate carboxylase. J Exp Bot 36: 610–622

    CAS  Google Scholar 

  • Macfarlane JJ, Raven JA (1989) Quantitative determination of the unstirred layer permeability and kinetic parameters of RUBISCO inLemanea mamillosa. J Exp Bot 40: 321–327

    CAS  Google Scholar 

  • Macfarlane JJ, Raven JA (1990) C, N and P nutrition ofLemanea mamillosa Kut3 (Batrachospermales, Rhodophyta) in the Dighty Burn, Angus Scotland. Plant Cell Environ 13: 1–13

    CAS  Google Scholar 

  • Mook WG, Bommerson JC, Staverman WH (1974) Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide. Earth Plan Sci Lett 22: 169–176

    Article  CAS  Google Scholar 

  • O'Leary MH (1984) Measurement of the isotopic fractionation associated with diffusion of carbon dioxide in aqueous solution. J Phys Chem 88: 823–825

    Google Scholar 

  • O'Leary MH (1989) Multiple isotope effects on enzyme-catalysed reactions. Annu Rev Biochem 58: 377–401

    Article  PubMed  Google Scholar 

  • Osmond CB, Valaane N, Haslam SM, Uotila P, Roksandic Z (1980) Comparisons of δ13C values in leaves of aquatic macrophytes from different habitats in Britain and Finland; some implications for photosynthetic processes in aquatic plants. Oecologia 50: 117–124

    Google Scholar 

  • Peisker M (1982) The effect of CO2 leakage from bundle sheath cells on carbon isotope discrimination. Photosynthetica 16: 533–541

    CAS  Google Scholar 

  • Raven JA (1984) Energetics and Transport in Aquatic Plants. A.R. Liss, New York

    Google Scholar 

  • Raven JA (1990) The use of isotopes in estimating respiration and photosynthesis in microalgae. Mar Microb Food Webs 4: 59–86

    Google Scholar 

  • Raven JA (1991) Implications of inorganic C utilization: ecology, evolution and geochemistry. Can J Bot 69: 908–924

    CAS  Google Scholar 

  • Raven JA, Farquhar GD (1990) The influence of N metabolism and organic acid synthesis on the natural abundance of C isotopes in plants. New Phytol 116: 505–529

    CAS  Google Scholar 

  • Raven JA, Johnston AM (1991a) Photosynthetic inorganic carbon assimilation byPrasiola stipitata (Prasioles, Chlorophyta) under emersed and submersed conditions: relationship to the taxonomy ofPrasiola. Br Phycol J 26: 247–257

    Google Scholar 

  • Raven JA, Johnston AM (1991b) Carbon assimilation mechanisms: implications for intensive culture of seaweeds. In: Garcia-Reina G, Pedersen M (eds) Proceedings of the Cost 48 Workshop on seaweed Biotechnology, Physiology and Intensive Cultivation, Gran Canaria, 1991, pp 151–166

  • Raven JA, Lucas WJ (1985) The energetics of carbon acquisition. In: Lucas WJ, Berry JA (eds) Inorganic carbon uptake by aquatic photosynthetic organisms. The American Society of Plant Physiologists, Rockville MD, pp 305–324

    Google Scholar 

  • Raven JA, Beardall J, Griffiths H (1982) Inorganic C-sources forLemanea, Cladophora, andRanunculus, in a fast-flowing stream: Measurements of gas exchange and of carbon isotope ratio and their ecological implications. Oecologia 53: 68–78

    Article  Google Scholar 

  • Raven JA, Macfarlane JJ, Griffiths H (1987) The application of carbon isotope discrimination techniques. In: Crawford RMM (ed) Plant Life in Aquatic and Amphibious Habitats, Blackwell, Oxford, pp 129–149

    Google Scholar 

  • Rebsdorf A, Thyssen N, Erlandsen M (1991) Regional and temporal variation in pH, alkalinity and carbon dioxide in Danish streams, related to soil type and land use. Freshw Biol 25: 419–435

    CAS  Google Scholar 

  • Reiskind JB, Bowes G (1991) The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. Proc Natl Acad Sci USA 88: 2883–2887

    CAS  PubMed  Google Scholar 

  • Reiskind JB, Seamon PT, Bowes G (1988) Alternative methods of photosynthetic carbon assimilation in marine macroalgae. Plant Physiol 87: 686–692

    CAS  Google Scholar 

  • Sharkey TD, Berry JA (1985) Carbon isotope fractionation of algae as influenced by an inducible CO2 concentrating mechanism. In: Lucas WJ, Berry JA (eds) Inorganic carbon uptake by aquatic photosynthetic organisms. The American Society of Plant Physiologists, Rockville MD, pp 389–401

    Google Scholar 

  • Skirrow G (1975) The dissolved gases-carbon dioxide. In: Riley JP, Skirrow G (eds) Chemical Oceanography Vol. 2, 2nd edn. Academic Press, London, pp 1–192

    Google Scholar 

  • Smith RG, Bidwell RGS (1989a) Mechanism of photosynthetic carbon dioxide uptake be the red macroalgaChondrus crispus. Plant Physiol 89: 93–99

    CAS  Google Scholar 

  • Smith RG, Bidwell RGS (1989b) Inorganic carbon uptake by photosynthetically active protoplasts of the red macroalgaChondrus crispus. Mar Biol 102: 1–4

    CAS  Google Scholar 

  • Smith SV (1985) Physical, chemical and biological characteristics of CO2 gas flux across the air-water interface. Plant Cell Environ 8: 387–398

    CAS  Google Scholar 

  • Spence DHN, Maberly SC (1985) Occurrence and ecological importance of HCO -3 use among aquatic higher plants. In: Lucas WJ, Berry JA (eds) Inorganic carbon uptake by aquatic photosynthetic organisms. The American Society of Plant Physiologists, Rockville MD, pp 125–143

    Google Scholar 

  • Surif MB, Raven JA (1989) Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and Laminariales (Phaeophyta): ecological and taxonomic implication. Oecologia 78: 97–105

    Article  Google Scholar 

  • Surif MB, Raven JA (1990) Photosynthetic gas exchange under emersed conditions in eulittoral and normally submersed members of the Fucales and the Laminariales: interpretation in relation to C isotope ratio and N and water use efficiency. Oecologia 82: 68–80

    Article  Google Scholar 

  • Takahashi K, Wada E, Sakamoto M (1990) Carbon isotope discrimination by phytoplankton and photosynthetic bacteria in monomictic Lake Fukami-ike. Arch Hydrobiol 120: 197–210

    Google Scholar 

  • Truchot J-P, Duhamel-Jouve A (1980) Oxygen and carbon dioxide in the marine intertidal environment: diurnal and tidal changes in rockpools. Resp Physiol 39: 241–254

    CAS  Google Scholar 

  • Wefer G, Killingley JS (1986) Carbon isotopes in organic matter from a benthic algaHalimeda incrassata (Bermuda): effects of light intensity. Chem Geol (Isotopes Geosciences Section) 59: 321–326

    CAS  Google Scholar 

  • Wiencke C, Fischer G (1990) Growth and stable carbon isotope composition of cold-water macroalgae in relation to light and temperature. Mar Ecol Prog Ser 65: 283–292

    Google Scholar 

  • Ye LX, Ritz DW Fenton GE, Lewis ME (1991) Tracing the influence on sediments of organic waste from a salmonid farm using stable isotope analysis. J Exp Mar Biol Ecol 145: 161–174

    Article  Google Scholar 

  • Ziegler H (1979) Diskriminierung von Kohlenstoff- und Wasserstoffisotopen: Zusammenhänge mit dem Photosynthesemechanismus und den Standartbedingungen. Ber Dtsch Bot Ges 92: 169–184

    CAS  Google Scholar 

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Maberly, S.C., Raven, J.A. & Johnston, A.M. Discrimination between12C and13C by marine plants. Oecologia 91, 481–492 (1992). https://doi.org/10.1007/BF00650320

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