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Journal of Oceanography

, Volume 67, Issue 4, pp 427–437 | Cite as

Production and bacterial decomposition of dissolved organic matter in a fringing coral reef

  • Yasuaki Tanaka
  • Hiroshi Ogawa
  • Toshihiro Miyajima
Original Article

Abstract

The concentrations of dissolved organic carbon and nitrogen (DOC and DON, respectively) were measured in Shiraho fringing reef (Japan), using a high-temperature catalytic-oxidation method. When the seawater on the reef flat (shallow lagoon) was isolated from the surrounding ocean due to the low tide, the concentrations of DOC and DON on the reef flat were 66–75 and 4.8–5.7 μmol l−1, respectively. The DOC and DON concentrations were higher than those of the adjacent outer ocean (57–58 and 3.8 μmol l−1, respectively), suggesting that the coral reef functioned as a net source of dissolved organic matter for the surrounding ocean. In order to investigate long-term bacterial decomposition of the reef-derived DOC (RF-DOC), the seawater samples collected on the reef flat and at the adjacent ocean were incubated in the dark for 1 year. Regression analysis using an exponential curve that considered two degradability pools (labile and refractory) fitted the mineralization of the RF-DOC very well (r 2 > 0.89). According to the regression analysis, the DOC produced on the reef flat was composed of the labile fraction of 63–94% (average 77%) and the refractory fraction of 6–37% (average 23%). It was concluded that some of the DOC that was produced in the coral reef ecosystem was exported to the surrounding ocean if the reef flat had a water residence time less than several months. The exported organic matter may support microbial communities in the ocean as an energy source.

Keywords

DOC DON POC PON Coral reefs Production Mineralization C:N ratio Bacteria Refractory organic matter 

Notes

Acknowledgments

We are grateful to two anonymous reviewers who provided helpful comments to improve this article. This study was financially supported by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists.

References

  1. Atkinson MJ, Falter JL (2003) Coral reefs. In: Black KD, Shimmield GB (eds) Biogeochemistry of marine systems. Blackwell, Oxford, pp 40–64Google Scholar
  2. Benner R (2002) Chemical composition and reactivity. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic, San Diego, pp 59–90CrossRefGoogle Scholar
  3. Bronk DA (2002) Dynamics of DON. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic, San Diego, pp 153–247CrossRefGoogle Scholar
  4. Carlson C (2002) Production and removal processes. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic, San Diego, pp 91–151CrossRefGoogle Scholar
  5. Conan P, Søndergaard M, Kragh T, Thingstad F, Pujo-Pay M, Williams PJ le B, Markager S, Cauwet G, Borch NH, Evan D, Riemann B (2007) Partitioning of organic production in marine plankton communities: the effects of inorganic nutrient ratios and community composition on new dissolved organic matter. Limnol Oceanogr 52:753–765Google Scholar
  6. Delesalle B, Buscail R, Carbonne J, Courp T, Dufour V, Heussner S, Monaco A, schrimm M (1998) Direct measurements of carbon and carbonate export from a coral reef ecosystem (Moorea Island, French Polynesia). Coral Reefs 17:121–132CrossRefGoogle Scholar
  7. Ferrier-Pagès C, Furla P (2001) Pico- and nanoplankton biomass and production in the two largest atoll lagoons of French Polynesia. Mar Ecol Prog Ser 211:63–76CrossRefGoogle Scholar
  8. Ferrier-Pagès C, Leclercq N, Jaubert J, Pelegrí SP (2000) Enhancement of pico- and nanoplankton growth by coral exudates. Aquat Microb Ecol 21:203–209CrossRefGoogle Scholar
  9. Gattuso JP, Pichon M, Delesalle B, Canon C, Frankignoulle M (1996) Carbon fluxes in coral reefs. I. Lagrangian measurement of community metabolism and resulting air–sea CO2 disequilibrium. Mar Ecol Prog Ser 145:109–121CrossRefGoogle Scholar
  10. Gattuso JP, Frankignoulle M, Wollast R (1998) Carbon and carbonate metabolism in coastal aquatic ecosystems. Annu Rev Ecol Syst 29:405–434CrossRefGoogle Scholar
  11. Haas AF, Wild C (2010) Composition analysis of organic matter released by cosmopolitan coral reef-associated green algae. Aquat Biol 10:131–138Google Scholar
  12. Hansell DA, Williams PM, Ward BB (1993) Results and observations from the measurement of DOC and DON in seawater using a high-temperature catalytic oxidation technique. Mar Chem 41:195–202CrossRefGoogle Scholar
  13. Hata H, Kudo S, Yamano H, Kurano N, Kayanne H (2002) Organic carbon flux in Shiraho coral reef (Ishigaki Island, Japan). Mar Ecol Prog Ser 232:129–140CrossRefGoogle Scholar
  14. Herndl GJ, Peter P (1989) Potential microbial utilization rates of sublittoral gastropod mucus trails. Limnol Oceanogr 34:780–784CrossRefGoogle Scholar
  15. Hopkinson CS, Fry B, Nolin AL (1997) Stoichiometry of dissolved organic matter dynamics on the continental shelf of the northeastern USA. Cont Shelf Res 17:473–489CrossRefGoogle Scholar
  16. Kähler P, Bjørnsen PK, Lochete K, Antia A (1997) Dissolved organic matter and its utilization by bacteria during spring in the Southern Ocean. Deep-Sea Res II 44:341–353CrossRefGoogle Scholar
  17. Karl DM, Hebel DV, Björkman K, Letelier RM (1998) The role of dissolved organic matter release in the productivity of the oligotrophic North Pacific Ocean. Limnol Oceanogr 43:1270–1286CrossRefGoogle Scholar
  18. Kayanne H, Hata H, Kudo S, Yamano H, Watanabe A, Ikeda Y, Nozaki K, Kato K, Negishi A, Saito H (2005) Seasonal and bleaching-induced changes in coral reef metabolism and CO2 flux. Glob Biogeochem Cycles 19:GB3015Google Scholar
  19. Lønborg C, Davidson K, Álvarez-Salgado XA, Miller AEJ (2009) Bioavailability and bacterial degradation rates of dissolved organic matter in a temperate coastal area during an annual cycle. Mar Chem 113:219–226CrossRefGoogle Scholar
  20. Marañón E, Cermeño P, Fernández E, Rodríguez J, Zabala L (2004) Significance and mechanisms of photosynthetic production of dissolved organic carbon in a coastal eutrophic ecosystem. Limnol Oceanogr 49:1652–1666CrossRefGoogle Scholar
  21. Meikle P, Richards GN, Yellowlees D (1988) Structural investigations on the mucus from six species of coral. Mar Biol 99:187–193CrossRefGoogle Scholar
  22. Miyajima T, Koike I, Yamano H, Iizumi H (1998) Accumulation and transport of seagrass-derived organic matter in reef flat sediment of Green Island, Great Barrier Reef. Mar Ecol Prog Ser 175:251–259CrossRefGoogle Scholar
  23. Miyajima T, Hata H, Umezawa Y, Kayanne H, Koike I (2007a) Distribution and partitioning of nitrogen and phosphorus in a fringing reef lagoon of Ishigaki Island, northwestern Pacific. Mar Ecol Prog Ser 341:45–57CrossRefGoogle Scholar
  24. Miyajima T, Tanaka Y, Koike I, Yamano H, Kayanne H (2007b) Evaluation of spatial correlation between nutrient exchange rates and benthic biota in a reef-flat ecosystem by GIS-assisted flow-tracking. J Oceanogr 63:643–659CrossRefGoogle Scholar
  25. Moran MA, Zepp RG (1997) Role of photoreactions in the formation of biologically labile compounds from dissolved organic matter. Limnol Oceanogr 42:1307–1316CrossRefGoogle Scholar
  26. Nakajima R, Yoshida T, Azman BAR, Zaleha K, Othman BHR, Toda T (2009) In situ release of coral mucus by Acropora and its influence on the heterotrophic bacteria. Aquat Ecol 43:815–823CrossRefGoogle Scholar
  27. Nakajima R, Yoshida T, Fujita K, Nakayama A, Fuchinoue Y, Othman BHR, Toda T (2010) Release of particulate and dissolved organic carbon by the scleractinian coral Acropora formosa. Bull Mar Sci 86:861–870CrossRefGoogle Scholar
  28. Nakamura T, Nakamori T (2009) Estimation of photosynthesis and calcification rates at a fringing reef by accounting for diurnal variations and the zonation of coral reef communities on reef flat and slope: a case study for the Shiraho reef, Ishigaki Island, southwest Japan. Coral Reefs 28:229–250CrossRefGoogle Scholar
  29. Ogawa H, Tanoue E (2003) Dissolved organic matter in oceanic waters. J Oceanogr 59:129–147CrossRefGoogle Scholar
  30. Ogawa H, Fukuda R, Koike I (1999) Vertical distributions of dissolved organic carbon and nitrogen in the Southern Ocean. Deep-Sea Res I 46:1809–1826CrossRefGoogle Scholar
  31. Ogawa H, Amagai Y, Koike I, Kaiser K, Benner R (2001) Production of refractory dissolved organic matter by bacteria. Science 292:917–920CrossRefGoogle Scholar
  32. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14CrossRefGoogle Scholar
  33. Rochelle-Newall EJ, Torréton JP, Mari X, Pringault O (2008) Phytoplankton-bacterioplankton coupling in a subtropical South Pacific coral reef lagoon. Aquat Microb Ecol 50:221–229CrossRefGoogle Scholar
  34. Sharp JH (2002) Analytical methods for total DOM pools. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic, San Diego, pp 35–58CrossRefGoogle Scholar
  35. Shibata A, Goto Y, Saito H, Kikuchi T, Toda T, Taguchi S (2006) Comparison of SYBR Green I and SYBR Gold stains for enumerating bacteria and viruses by epifluorescence microscopy. Aquat Microb Ecol 43:223–231CrossRefGoogle Scholar
  36. Suzuki R, Ishimaru T (1990) An improved method for the determination of phytoplankton chlorophyll using N,N dimethylformamide. J Oceanogr 46:190–194Google Scholar
  37. Tanaka Y, Miyajima T, Umezawa Y, Hayashibara T, Ogawa H, Koike I (2009a) Net release of dissolved organic matter by the scleractinian coral Acropora pulchra. J Exp Mar Biol Ecol 377:101–106CrossRefGoogle Scholar
  38. Tanaka Y, Miyajima T, Ogawa H (2009b) Bacterial degradability of dissolved organic carbon in coral mucus. Proceedings of the 11th International Coral Reef Symposium, pp 945–949Google Scholar
  39. Tanaka Y, Miyajima T, Ogawa H (2010) Effects of nutrient enrichment on the release of dissolved organic carbon and nitrogen by the scleractinian coral Montipora digitata. Coral Reefs 29:675–682CrossRefGoogle Scholar
  40. Tanaka Y, Miyajima T, Watanabe A, Nadaoka K, Yamamoto T, Ogawa H (2011) Distribution of dissolved organic carbon and nitrogen in a coral reef. Coral Reefs 30:533–541CrossRefGoogle Scholar
  41. Umezawa Y, Miyajima T, Kayanne H, Koike I (2002) Significance of groundwater nitrogen discharge into coral reefs at Ishigaki Island, southwest of Japan. Coral Reefs 21:346–356Google Scholar
  42. Vacelet E, Thomassin BA (1991) Microbial utilization of coral mucus in long term in situ incubation over a coral reef. Hydrobiologia 211:19–32CrossRefGoogle Scholar
  43. Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jørgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70CrossRefGoogle Scholar
  44. Wild C, Woyt H, Huettel M (2005) Influence of coral mucus on nutrient fluxes in carbonate sands. Mar Ecol Prog Ser 287:87–98CrossRefGoogle Scholar
  45. Yahel G, Sharp JH, Marie D, Häse C, Genin A (2003) In situ feeding and element removal in the symbiont-bearing sponge Theonella swinhoei: bulk DOC is the major source for carbon. Limnol Oceanogr 48:141–149CrossRefGoogle Scholar
  46. 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

© The Oceanographic Society of Japan and Springer 2011

Authors and Affiliations

  • Yasuaki Tanaka
    • 1
    • 2
  • Hiroshi Ogawa
    • 1
  • Toshihiro Miyajima
    • 1
  1. 1.Marine Biogeochemistry Laboratory, Atmosphere and Ocean Research InstituteThe University of TokyoKashiwaJapan
  2. 2.Tropical Biosphere Research CenterUniversity of the RyukyusOkinawaJapan

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