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Stable nitrogen isotope composition in sedimentary organic matter as a potential proxy of nitrogen sources for primary producers at a fringing coral reef

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Abstract

The stable nitrogen isotope ratio (δ 15N) in macroalgae is effectively used as a time-integrated bioindicator to record nitrogen sources for primary producers during their growing periods in aquatic ecosystems. However, the utility of this tool is limited because the occurrence of these organisms is often restricted in space and time. To investigate the potential of chemical composition in sedimentary organic matter (SOM) as a proxy for time-integrated environmental conditions, nitrogen (N) and carbon (C) contents and their stable isotope ratios (δ 15N and δ 13C) were determined, and systematically cross-checked against corresponding values in macroalgae at the Shiraho fringing reef in Okinawa, Japan. Preliminary trials showed that δ 15N in SOM processed by the “wash-out method” for δ 13C analysis yielded similar δ 15N values to the bulk sediment, despite the loss of some SOM during the process. The amounts of organic matter and the ratio of the HCl-insoluble portion were variable within the reef, probably reflecting local vegetation and subsequent decomposition. The distribution of δ 15N and δ 13C in SOM showed similar trends to those of macroalgae, with mostly constant differences of 1.4‰ and −6.7‰, respectively. These differences throughout the reef appeared to be explained in terms of mixed contributions from macrophyte and epibenthic microalgae growing in different seasons and years, with their debris undergoing diagenetic alteration. Therefore, macroalgae and SOM δ-values can be used in a complementary manner, over various time scales, as indicators of the integrated effect of dissolved inorganic nitrogen (DIN) sources on coral reef ecosystems.

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References

  • Altabet, M. A. and R. Francois (1994): Sedimentary nitrogen isotopic ratio as a recorder for surface ocean nitrate utilization. Global Biogeochem. Cycles, 8, 103–116.

    Article  Google Scholar 

  • Atkinson, M. J. (1988): Are coral reefs nutrients-limited? Proc. 6th Int. Coral Reef Symp., 1, 57–66.

    Google Scholar 

  • Aumont, O., E. Maier-Reimer, S. Blain and P. Monfray (2003): An ecosystem model of the global ocean including Fe, Si, P colimitations. Global Biogeochem. Cycles, 17, 1060, doi:10.1029/2001GB001745.

    Article  Google Scholar 

  • Brenner, M., T. J. Whitmore, J. H. Curtis, D. A. Hodell and C. L. Schelske (1999): Stable isotope (δ 13C and δ 15N) signatures of sedimented organic matter as indicators of historic lake trophic state. J. Paleolimnol., 22, 205–221.

    Article  Google Scholar 

  • Bunn, S. E., N. R. Loneragan and M. A. Kempster (1995): Effects of acid washing on stable-isotope ratios of C and N in penaeid shrimp and seagrass, implications for food-web studies using multiple stable isotopes. Limnol. Oceanogr., 40, 622–625.

    Google Scholar 

  • Campbell, S. (2001): Ammonium requirements of fast-growing ephemeral macroalgae in a nutrient-enriched marine embayment (Port Phillip Bay, Australia). Mar. Ecol. Prog. Ser., 209, 99–107.

    Article  Google Scholar 

  • Charpy-Roubaud, C. J., C. Charpy and L. Lemasson (1988): Benthic and planktonic primary production of an open atoll lagoon. Proc 6th Int. Coral Reef Symp., 2, 551–556.

    Google Scholar 

  • Coffroth, M. A. (1990): Mucus sheet formation on poritid corals: an evaluation of coral mucus as a nutrient source on reefs. Mar. Biol., 105, 39–49.

    Article  Google Scholar 

  • Daumas, R. and B. A. Thomassin (1977): Protein fractions in coral and zoantharian mucus, possible evolution in coral reef environment. Proc. 3rd Int. Coral Reef Symp., 1, 517–524.

    Google Scholar 

  • Duarte, C. M. (1995): Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia, 41, 87–112.

    Google Scholar 

  • Einav, R., S. Breckle and S. Beer (1995): Ecophysiological adaptation strategies of some intertidal marine macroalgae of the Israeli Mediterranean coast. Mar. Ecol. Prog. Ser., 125, 219–228.

    Article  Google Scholar 

  • Finlay, J. C. (2004): Patterns and controls of lotic algal stable carbon isotope ratios. Limnol. Oceanogr., 49, 850–861.

    Google Scholar 

  • Fong, P., K. Kamer, K. E. Boyer and K. A. Boyle (2001): Nutrient content of macroalgae with differing morphologies may indicate sources of nutrients for tropical marine systems. Mar. Ecol. Prog. Ser., 220, 137–152.

    Article  Google Scholar 

  • Freudenthal, T., T. Wagner, F. Wenzhofer, M. Zabel and G. Wefer (2001): Early diagenesis of organic matter from sediments of the eastern subtropical Atlantic: Evidence from stable nitrogen and carbon isotopes. Geochim. Cosmochim. Acta, 65, 1795–1808.

    Article  Google Scholar 

  • Furnas, M., A. Mitchell and M. Skuza (1997): Shelf-scale nitrogen and phosphorus budgets for the central Great Barrier Reef. Proc. 8th Int. Coral Reef Symp., 1, 809–814.

    Google Scholar 

  • Galloway, J. N. and E. Cowling (2002): Reactive nitrogen and the world: 200 years of change. AMBIO, 31, 64–71.

    Article  Google Scholar 

  • Gartner, A., P. Lavery and A. J. Smit (2002): Use of δ 15N signatures of different functional forms of macroalgae and filter-feeders to reveal temporal and spatial patterns in sewage dispersal. Mar. Ecol. Prog. Ser., 235, 63–73.

    Article  Google Scholar 

  • Goñi, M., M. J. Teixeira and D. W. Perkey (2003): Sources and distribution of organic matter in a river-dominated estuary (Winyah Bay, SC, USA). Estuar. Coast. Shelf Sci., 57, 1023–1048.

    Article  Google Scholar 

  • Gu, B., C. L. Schelske and M. Brenner (1996): Relationship between sediment and plankton isotope ratios (delta C-13 and delta N-15) and primary productivity in Florida lakes. Can. J. Fish Aquat. Sci., 53, 875–883.

    Article  Google Scholar 

  • Harii, S. and H. Kayanne (2003): Larval dispersal, recruitment, and adult distribution of the brooding stony octocoral Heliopora coerulea on Ishigaki Island, southwest Japan. Coral Reefs, 22, 188–196.

    Article  Google Scholar 

  • Harris, D., W. R. Horwáth and C. van Kessel (2001): Acid fumigation of soils to remove carbonates prior to total organic carbon or carbon-13 isotopic analysis. Soil Sci. Soc. Am. J., 65, 1853–1856.

    Google Scholar 

  • Hata, H., S. Kudo, H. Yamano, N. Kurano and H. Kayanne (2002): Organic carbon flux in Shiraho coral reef (Ishigaki Island, Japan). Mar. Ecol. Prog. Ser., 232, 129–140.

    Article  Google Scholar 

  • Huettel, M., W. Ziebis and S. Forster (1996): Flow-induced uptake of particulate matter in permeable sediments. Limnol. Oceanogr., 41, 309–322.

    Google Scholar 

  • Hughes, T. P. and J. H. Connell (1999): Multiple stressors on coral reefs: A long term perspective. Limnol. Oceanogr., 44, 932–940.

    Google Scholar 

  • Hwang, R., C. C. Tsai and T. M. Lee (2004): Assessment of temperature and nutrient limitation on seasonal dynamics among species of Sargassum from a coral reef in southern Taiwan. J. Phycol., 40, 463–473.

    Article  Google Scholar 

  • Ismail, M., T. Kimura, Y. Suzuki and M. Tsuchiya (2005): Seasonal and spatial variations of total mass flux around coral reefs in the Southern Ryukyus, Japan. J. Oceanogr., 61, 631–644.

    Article  Google Scholar 

  • Jacob, U., K. Mintenbeck, T. Brey, R. Knust and K. Beyer (2005): Stable isotope food web studies: a case for standardized sample treatment. Mar. Ecol. Prog. Ser., 287, 251–253.

    Article  Google Scholar 

  • Jones, R., L. King, M. M. Dent, S. C. Maberly and C. E. Gibson (2004): Nitrogen stable isotope ratios in surface sediments, epilithon and macrophytes from upland lakes with differing nutrient status. Freshwater Biol., 49, 382–391.

    Article  Google Scholar 

  • Kayanne, H., Y. Tanaka, Y. Ide and F. Akimoto (1998): Biomass of primary producers at the Shiraho Reef, Ishigaki Island. Proc. 1st Japanese Coral Reef Society, Tokyo, p. 44.

  • Kim, K., T. S. Choi, J. H. Kim, T. Han, H. W. Shin and D. J. Garbary (2004): Physiological ecology and seasonality of Ulva pertusa on a temperate rocky shore. Phycologia, 43, 483–492.

    Article  Google Scholar 

  • Kirchman, D. L. (2000): Uptake and regeneration of inorganic nutrients by marine heterotrophic bacteria. In Microbial Ecology of the Oceans, ed. by D. L. Kirchman, John Wiley & Sons, Inc., 542 pp.

  • Klap, V., M. A. Hemminga and J. J. Boon (2000): Retention of lignin in seagrasses: angiosperms that returned to the sea. Mar. Ecol. Prog. Ser., 194, 1–11.

    Article  Google Scholar 

  • Kuramoto, T. and M. Minagawa (2001): Stable carbon and nitrogen isotopic characterization of organic matter in a mangrove ecosystem on the southwestern coast of Thailand. J. Oceanogr., 57, 421–431.

    Article  Google Scholar 

  • Lapointe, B. E. (1997): Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and Southeast Florida. Limnol. Oceanogr., 42, 1119–1131.

    Google Scholar 

  • Lehmann, M. F., S. M. Bernasconi, A. Barbieri and J. A. McKenzie (2002): Preservation of organic matter and alteration of its carbon and nitrogen isotope composition during simulated and in situ early sedimentary diagenesis. Geochim. Cosmochim. Acta, 66, 3573–3584.

    Article  Google Scholar 

  • Leichter, J. J., H. L. Stewart and S. L. Miller (2003): Episodic nutrient transport to Florida coral reefs. Limnol. Oceanogr., 48, 1394–1407.

    Google Scholar 

  • Lohse, L., R. Kloosterhuis, H. de Stigter, W. Helder, W. van Raaphorst and T. van Weering (2000): Carbonate removal by acidification causes loss of nitrogenous compounds in continental margin sediments. Mar. Chem., 69, 193–201.

    Article  Google Scholar 

  • Maberly, S. C., J. A. Raven and A. M. Johnston (1992): Discrimination between 12C and 13C by marine plants. Oecologia, 91, 481–492.

    Article  Google Scholar 

  • Macko, S. A., M. Engel and Y. Qian (1994): Early diagenesis and organic matter preservation? a molecular stable carbon isotope perspective. Chem. Geol., 114, 365–379.

    Article  Google Scholar 

  • McClelland, J. W. and I. Valiela (1998): Linking nitrogen in estuarine producers to land-derived sources. Limnol. Oceanogr., 43, 577–585.

    Google Scholar 

  • McCook, L. J., J. Jompa and G. Diaz-Pulido (2001): Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs, 19, 400–417.

    Article  Google Scholar 

  • Midwood, A. and T. W. Boutton (1998): Soil carbonate decomposition by acid has little effect on δ 13C of organic matter. Soil Biol. Biochem., 30, 1301–1307.

    Article  Google Scholar 

  • Minagawa, M. and E. Wada (1984): Stepwise enrichment of 15N along food-chains: further evidence and the relation between δ 15N and animal age. Geochim. Cosmochim. Acta, 48, 1135–1140.

    Article  Google Scholar 

  • Mishima, Y., A. Hoshika and T. Tanimoto (1999): Deposition rates of terrestrial and marine organic carbon in the Osaka bay, Seto Inland Sea, Japan, determined using carbon and nitrogen stable isotope ratios in the sediment. J. Oceanogr., 55, 1–11.

    Article  Google Scholar 

  • Miyajima, T., I. Koike, H. Yamano and H. Iizumi (1998): Accumulation and transport of seagrass-derived organic matter in reef flat sediment of Green Island, Great Barrier Reef. Mar. Ecol. Prog. Ser., 175, 251–259.

    Article  Google Scholar 

  • Miyajima, T., M. Suzumura, Y. Umezawa and I. Koike (2001): Microbiological nitrogen transformation in carbonate sediments of coral-reef lagoon and associated seagrass beds. Mar. Ecol. Prog. Ser., 217, 273–286.

    Article  Google Scholar 

  • Miyajima, T., H. Hata, Y. Umezawa, H. Kayanne and I. Koike (2007a): Distribution and partitioning of nitrogen and phosphorus in a fringing reef lagoon of Ishigaki Island, northwestern Pacific. Mar. Ecol. Prog. Ser., 341, 45–57.

    Article  Google Scholar 

  • Miyajima, T., Y. Tanaka, I. Koike, H. Yamano and H. Kayanne (2007b): Evaluation of spatial correlation between nutrient exchange rates and benthic biota in a reef-flat ecosystem by GIS-assisted flow-tracking method. J. Oceanogr., 63, 643–659.

    Article  Google Scholar 

  • Pedersen, M. and J. Borum (1996): Nutrient control of algal growth in estuarine waters. Nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macroalgae. Mar. Ecol. Prog. Ser., 142, 261–272.

    Article  Google Scholar 

  • Prokopenko, M. G., D. E. Hammond, W. M. Berelson, J. M. Bernhard, L. Stott and R. Douglas (2006): Nitrogen cycling in the sediments of Santa Barbara basin and Eastern Subtropical North Pacific: Nitrogen isotopes, diagenesis and possible chemosymbiosis between two lithotrophs (Thioploca and Anammox)—“riding on a glider”. Earth Planet. Sci. Lett., 242, 186–204.

    Article  Google Scholar 

  • Sato, T., T. Miyajima, H. Ogawa, Y. Umezawa and I. Koike (2006): Temporal variability of stable carbon and nitrogen isotopic composition of size-fractionated particulate organic matter in the hypertrophic Sumida River Estuary of Tokyo Bay, Japan. Estuar. Coast. Shelf Sci., 68, 245–258.

    Article  Google Scholar 

  • Savage, C. (2005): Tracing the influence of sewage nitrogen in a coastal ecosystem using stable nitrogen isotopes. AMBIO, 34, 145–150.

    Article  Google Scholar 

  • Schaffelke, B. and D. W. Klumpp (1998): Short-term nutrient pulses enhance growth and photosynthesis of the coral reef macroalga Sargassum baccularia. Mar. Ecol. Prog. Ser., 170, 95–105.

    Article  Google Scholar 

  • Schmidt, M. W. I. and G. Gleixner (2005): Carbon and nitrogen isotope composition of bulk soils, particle-size fractions and organic material after treatment with hydrofluoric acid. Eur. J. Soil Sci., 56, 407–416.

    Article  Google Scholar 

  • Schrimm, M., R. Buscail and M. Adjeroud (2004): Spatial variability of the biogeochemical composition of surface sediments in an insular coral reef ecosystem: Moorea, French Polynesia. Estuar. Coast. Shelf Sci., 60, 515–528.

    Article  Google Scholar 

  • Schubert, C. J. and B. Nielsen (2000): Effects of decarbonation treatments on δ 13C values in marine sediments. Mar. Chem., 72, 55–59.

    Article  Google Scholar 

  • Schweizer, M., J. Fear and G. Cadisch (1999): Isotopic (13C) fractionation during plant residue decomposition and its implications for soil organic matter studies. Rapid Commu. Mass Sp., 13, 1284–1290.

    Article  Google Scholar 

  • Seitzinger, S. P. and C. Kroezek (1998): Global distribution of nitrous oxide production and N inputs in fresh water and coastal marine ecosystems. Global Biogeochem. Cycles, 12, 93–113.

    Article  Google Scholar 

  • Smith, J. E., C. L. Hunter, E. J. Conklin, R. Most, T. Sauvage, C. Squair and C. M. Smith (2004): Ecology of the Invasive Red Alga Gracilaria salicornia (Rhodophyta) on O’ahu, Hawai’i. Pacific Science, 58, 325–343.

    Article  Google Scholar 

  • Suhayda, J. N. and H. H. Roberts (1977): Wave action and sediment transport on fringing reefs. Proc. 3rd Int. Coral Reef Symp., 2, 65–70.

    Google Scholar 

  • Thomassin, B. A. and G. Cauwet (1985): Organic matter distribution in sediments of the Tuléar coral reef complexes. Proc. 5th Int. Coral Reef Symp., 3, 377–382.

    Google Scholar 

  • Tsuboi, Y. (2007): Dynamics of dissolved silicate and biogenic silica in tropical and subtropical river water. Master Thesis, Institute for Environmental Studies, The University of the Tokyo, 49 pp. (in Japanese with English abstract).

  • Umezawa, Y. (2004): Nutrient dynamics in tropical and subtropical coastal ecosystems assessed by δ 15N in macroalgae. Ph.D. Thesis, The University of Tokyo, 219 pp.

  • Umezawa, Y., T. Miyajima, I. Koike and H. Kayanne (2002a): Significance of groundwater nitrogen discharge into coral reefs at Ishigaki Island, southwest of Japan. Coral Reefs, 21, 346–356.

    Google Scholar 

  • Umezawa, Y., T. Miyajima, M. Yamamuro, H. Kayanne and I. Koike (2002b): Fine scale mapping of land-derived nitrogen in coral reefs, by δ 15N values in macroalgae. Limnol. Oceanogr., 47, 1405–1416.

    Google Scholar 

  • Umezawa, Y., T. Miyajima, Y. Tanaka, I. Koike and T. Hayashibara (2007): Variation in internal δ 15N and δ 13C distribution in the brown macroalgae Padina australis growing in subtropical oligotrophic waters. J. Phycol., 43, 437–448.

    Article  Google Scholar 

  • Vizzini, S. and A. Mazzola (2003): Seasonal variations in the stable carbon and nitrogen isotope ratios (13C/12C and 15N/14N) of primary producers and consumers in a western Mediterranean coastal lagoon. Mar. Biol., 142, 1009–1018.

    Google Scholar 

  • Wild, C., M. Huettel, A. Klueter, S. G. Kremb, M. Y. M. Rasheed and B. B. Jørgensen (2004): Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature, 428, 66–70.

    Article  Google Scholar 

  • Yamamuro, M. and H. Kayanne (1995): Rapid direct determination of organic carbon and nitrogen in carbonate-bearing sediments with a Yanaco MT-5 CHN analyzer. Limnol. Oceanogr., 40, 1001–1005.

    Google Scholar 

  • Yamamuro, M., M. Minagawa and H. Kayanne (1992): Preliminary observation on food webs in Shiraho coral reef as determined from carbon and nitrogen stable isotopes. Proc. 7th Int. Coral Reef Symp., 352–355.

  • Zieman, J. C., S. A. Macko and A. L. Mills (1984): Role of seagrasses and mangroves in estuarine food webs: temporal and spatial changes in stable isotope composition and amino acid content during decomposition. Bull. Mar. Sci., 35, 380–392.

    Google Scholar 

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Umezawa, Y., Miyajima, T. & Koike, I. Stable nitrogen isotope composition in sedimentary organic matter as a potential proxy of nitrogen sources for primary producers at a fringing coral reef. J Oceanogr 64, 899–909 (2008). https://doi.org/10.1007/s10872-008-0074-5

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