Coral Reefs

, Volume 32, Issue 4, pp 1103–1110 | Cite as

Heterogeneous dissolved organic nitrogen supply over a coral reef: first evidence from nitrogen stable isotope ratios

  • B. Thibodeau
  • T. Miyajima
  • I. Tayasu
  • A. S. J. Wyatt
  • A. Watanabe
  • N. Morimoto
  • C. Yoshimizu
  • T. Nagata
Report

Abstract

Dissolved organic nitrogen (DON) potentially plays a major role in sustaining the high productivity and biological diversity of coral reefs. However, data are scarce regarding sources and sinks of DON. This study, for the first time, determined the 15N isotopic composition of total dissolved nitrogen (δ15NTDN), reflecting the isotopic signature of DON, in the water column over a coral reef. The uniformity in δ15NTDN during high tide (3.2 ± 0.3 ‰) indicated that the DON was mainly derived from offshore waters. In contrast, higher spatial heterogeneity of δ15NTDN (3.1 ± 0.9 ‰) and DON concentrations during low tide indicated the existence of local DON sources patchily distributed over the reef. Low δ15NTDN values located mid-reef were indicative of DON release from organisms that obtained their N via N2 fixation, whereas high δ15NTDN appeared to reflect localized release of DON by organisms exposed to dissolved inorganic nitrogen with elevated 15N, such as from terrestrial and offshore inputs. Collectively, the results highlight the importance of spatial patterns in DON release from reef communities in the N cycling of coral reefs.

Keywords

Geochemistry Stable isotopes Nitrogen cycle Dissolved organic nitrogen Dinitrogen fixation Coral reefs 

Supplementary material

338_2013_1070_MOESM1_ESM.docx (33 kb)
Supplementary material 1 (DOCX 32 kb)
338_2013_1070_MOESM2_ESM.eps (1.1 mb)
Supplementary material 2 (EPS 1121 kb)
338_2013_1070_MOESM3_ESM.docx (20 kb)
Supplementary material 3 (DOCX 19 kb)

References

  1. Atkinson M (2011) Biogeochemistry of nutrients. In: Dubinsky Z, Stambler N (eds) Coral reefs: An ecosystem in transition. Springer, pp 199-206Google Scholar
  2. Atkinson M, Falter J (2003) Coral reefs. In: Black K, Shimmield G (eds) Biogeochemistry of marine systems. Sheffield Academic Press, pp 40-64Google Scholar
  3. Bourbonnais A, Lehmann MF, Waniek JJ, Schulz-Bull DE (2009) Nitrate isotope anomalies reflect N2 fixation in the Azores Front region (subtropical N-E Atlantic). J Geophys Res 114:C03003. doi:10.1029/2007JC004617 CrossRefGoogle Scholar
  4. Bronk DA, See JH, Bradley P, Killberg L (2007) DON as a source of bioavailable nitrogen for phytoplankton. Biogeosciences 4:283–296CrossRefGoogle Scholar
  5. Casciotti KL, Sigman DM, Hastings MG, Böhlke JK, Hilkert A (2002) Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method. Anal Chem 74:4905–4912PubMedCrossRefGoogle Scholar
  6. Charpy-Roubaud CJ, Charpy L, Cremoux JL (1990) Nutrient budget of the lagoonal waters in an open central south-Pacific atoll (Tikehau, Tuamotu, French-Polyniesia). Mar Biol 107:67–73CrossRefGoogle Scholar
  7. Fogel ML, Cifuentes LA (1993) Isotope fractionation during primary production. In: Engel MH, Macko SA (eds) Organic geochemistry. Plenum Press, New York, pp 73–98CrossRefGoogle Scholar
  8. Granger J, Sigman DM, Needoba JA, Harrison PJ (2004) Coupled nitrogen and oxygen isotope fractionation of nitrate during assimilation by cultures of marine phytoplankton. Limnol Oceanogr 49:1763–1773CrossRefGoogle Scholar
  9. Grasshoff K, Kremling K, Ehrhardt M (1999) Methods of seawater analysis. Weinheim, TorontoGoogle Scholar
  10. Haas AF, Wild C (2010) Composition analysis of organic matter released by cosmopolitan coral reef-associated green algae. Aquat Biol 10:131–138Google Scholar
  11. Hongo C, Kayanne H (2009) Holocene coral reef development under windward and leeward locations at Ishigaki Island, Ryukyu Islands, Japan. Sediment Geol 214:62–73CrossRefGoogle Scholar
  12. Johannes RE, McCloske Lr, Marsh JA, Marshall N, Maragos J, Alberts J, Betzer S, Clutter RI, Crabtree D, Helfrich P, Telek G, Wells JM, Webb KL, Wiebe W, Roth A, Sottile W, Smith S, Pomeroy LR, Pilson MEQ, Meyer J, Delia C, Dupaul WD, Kinzie RA (1972) Metabolism of some coral reef communities - team study of nutrient and energy flux at Eniwetok. Bioscience 22:541–543CrossRefGoogle Scholar
  13. Johannes RE, Wiebe WJ, Crossland CJ (1983) Three patterns of nutrient flux in a coral reef community. Mar Ecol Prog Ser 12:131–136CrossRefGoogle Scholar
  14. Kayanne H, Hirota M, Yamamuro M, Koike I (2005) Nitrogen fixation of filamentous cyanobacteria in a coral reef measured using three different methods. Coral Reefs 24:197–200CrossRefGoogle Scholar
  15. Kendall C, Elliott EM, Wankel SD (2007) Tracing anthropogenic inputs of nitrogen to ecosystems, Chapter 12. In: Michener RH, Lajtha K (eds) Stable isotopes in ecology and environmental science, 2nd edition. Blackwell Publishing, pp 375- 449Google Scholar
  16. Knapp AN, Sigman DM, Lipschultz F (2005) N isotopic composition of dissolved organic nitrogen and nitrate at the Bermuda Atlantic Time-series study site. Global Biogeochem Cycles 19:1-15 [10.1029/2010gb003878]Google Scholar
  17. Knapp AN, Sigman DM, Lipschultz F, Kustka AB, Capone DG (2011) Interbasin isotopic correspondence between upper-ocean bulk DON and subsurface nitrate and its implications for marine nitrogen cycling. Global Biogeochem Cycles 25 (4), GB4004, doi:10.1029/2010GB003878
  18. Knapp AN, Sigman DM, Kustka AB, Sanudo-Wilhelmy SA, Capone DG (2012) The distinct nitrogen isotopic compositions of low and high molecular weight marine DON. Mar Chem 136:24–33CrossRefGoogle Scholar
  19. Lehmann MF, Reichert P, Bernasconi SM, Barbieri A, McKenzie JA (2003) Modelling nitrogen and oxygen isotope fractionation during denitrification in a lacustrine redox-transition zone. Geochim Cosmochim Acta 67:2529–2542CrossRefGoogle Scholar
  20. Leichter JJ, Paytan A, Wankel S, Hanson K, Miller S, Altabet MA (2007) Nitrogen and oxygen isotopic signatures of subsurface nitrate seaward of the Florida Keys reef tract. Limnol Oceanogr 52:1258–1267CrossRefGoogle Scholar
  21. Muscatine L, Porter JW (1977) Reef corals - mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460CrossRefGoogle Scholar
  22. Odum HT, Odum EP (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok atoll. Ecol Monogr 25:291–320CrossRefGoogle Scholar
  23. Reynaud S, Martinez P, Houlbreque F, Billy I, Allemand D, Ferrier-Pages C (2009) Effect of light and feeding on the nitrogen isotopic composition of a zooxanthellate coral: role of nitrogen recycling. Mar Ecol-Prog Ser 392:103–110CrossRefGoogle Scholar
  24. Sammarco PW, Risk MJ, Schwarcz HP, Heikoop JM (1999) Cross-continental shelf trends in coral delta N-15 on the Great Barrier Reef: further consideration of the reef nutrient paradox. Mar Ecol-Prog Ser 180:131–138CrossRefGoogle Scholar
  25. Schlarbaum T, Daehnke K, Emeis K (2010) Turnover of combined dissolved organic nitrogen and ammonium in the Elbe estuary/NW Europe: Results of nitrogen isotope investigations. Mar Chem 119:91–107CrossRefGoogle Scholar
  26. Sigman DM, Casciotti KL, Andreani M, Barford C, Galanter M, Böhlke JK (2001) A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal Chem 73:4145–4153PubMedCrossRefGoogle Scholar
  27. Solorzano L, Sharp JH (1980) Determination of total dissolved nitrogen in natural-waters. Limnol Oceanogr 25:751–754CrossRefGoogle Scholar
  28. Suzuki Y, Casareto BE (2011) The role of dissolved organic nitrogen (DON) in coral biology and reef ecology. In: Dubinsky Z, Stambler N (eds) Coral reefs: An ecosystem in transition. Springer, pp 207-214Google Scholar
  29. Tanaka Y, Miyajima T, Umezawa Y, Hayashibara T, Ogawa H, Koike I (2009) Net release of dissolved organic matter by the scleractinian coral Acropora pulchra. J Exp Mar Biol Ecol 377:101–106CrossRefGoogle Scholar
  30. Thibodeau B, Hélie JF, Lehmann MF (2013) Variations of the nitrate isotopic composition in the St. Lawrence River caused by seasonal changes in atmospheric nitrogen inputs. Biogeochemistry, 10.1007/s10533-013-9834-4
  31. Umezawa Y, Miyajima T, Yamamuro M, Kayanne H, Koike I (2002) Fine-scale mapping of land-derived nitrogen in coral reefs by delta N-15 in macroalgae. Limnol Oceanogr 47:1405–1416CrossRefGoogle Scholar
  32. Wankel SD, Kendall C, Francis CA, Paytan A (2006) Nitrogen sources and cycling in the San Francisco Bay estuary: A nitrate dual isotopic composition approach. Limnol Oceanogr 51:1654–1664CrossRefGoogle Scholar
  33. Webb KL, Dupaul WD, Wiebe W, Sottile W, Johannes RE (1975) Enewetak (Eniwetok) atoll - aspects of nitrogen cycle on a coral-reef. Limnol Oceanogr 20:198–210CrossRefGoogle Scholar
  34. Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret FE, Postle AD, Achterberg EP (2012) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Change doi:10.1038/nclimate1661
  35. Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jorgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70PubMedCrossRefGoogle Scholar
  36. Wyatt ASJ, Falter JL, Lowe RJ, Humphries S, Waite AM (2012) Oceanographic forcing of nutrient uptake and release over a fringing coral reef. Limnol Oceanogr 57:401–419CrossRefGoogle Scholar
  37. Ziegler S, Benner R (1999) Dissolved organic carbon cycling in a subtropical seagrass-dominated lagoon. Mar Ecol-Prog Ser 180:149–160CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • B. Thibodeau
    • 1
    • 4
  • T. Miyajima
    • 1
  • I. Tayasu
    • 2
  • A. S. J. Wyatt
    • 1
  • A. Watanabe
    • 3
  • N. Morimoto
    • 1
  • C. Yoshimizu
    • 2
  • T. Nagata
    • 1
  1. 1.Atmosphere and Ocean Research InstituteThe University of TokyoKashiwaJapan
  2. 2.Center for Ecological ResearchKyoto UniversityOtsuJapan
  3. 3.Graduate School of Information Science and EngineeringTokyo Institute of TechnologyTokyoJapan
  4. 4.Academy of Sciences, Humanities and Literature, Mainzc/o Helmholtz Centre for Oceanographic Research (GEOMAR)KielGermany

Personalised recommendations