Skip to main content
SpringerLink
Log in

Dinitrogen fixation by exposed communities on the rim of Tikehau atoll (Tuamotu Archipelago, French Polynesia)

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Various types of sub-aerially exposed microbial mats, including emergent mats, beach sand, beach rock and Kopara mats, are widespread on the 78 km (25 km2) of rim surrounding the Tikehau atoll lagoon. These mats form laminated accretions or diffuse microbial communities growing under high insolation and temperatures, and are therefore subject to desiccation. Both heterocystous and non-heterocystous cyanobacteria occur in these mats. Using acetylene reduction techniques, nitrogenase activity was observed at all sites over a period of 5 years and was 3–17 times higher during daylight than at night in all communities except for beach rock. 15N2 measurements indicated a molar ratio of acetylene reduction to N2 fixed of 1.6 for all exposed communities. Estimated N2 fixation ranged from 1.44 to 8.0 mg N m−2 day−1 in these exposed communities (mean of 4.66 mg N m−2 day−1) with beachrock showing the highest rates. For the whole reef rim, daily N2 fixation amounted to 98.42 kg N day−1 which represents 28% of the rate of fixation in the entire lagoon (area 400 km2).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Bautista MF, Paerl HW (1985) Diel N2 fixation in an intertidal marine cyanobacterial mat community. Mar Chem 16:369–377

    Article  CAS  Google Scholar 

  • Bohlool BB, Wiebe WJ (1978) Nitrogen-fixing communities in an intertidal ecosystem. Can J Microbiol 24:932–938

    PubMed  CAS  Google Scholar 

  • Brenowitz S, Castenholz RW (1997) Long term effects of UV and visible irradiance on natural populations of a scytonemin-containing cyanobacterium (Calothrix sp.). FEMS Microbiol Ecol 34:343–352

    Google Scholar 

  • Burris RH (1976) Nitrogen fixation by blue-green algae of the Lizard Island area of the Great Barrier Reef. Aust J Plant Physiol 3:41–51

    Article  CAS  Google Scholar 

  • Capone DG (1983) Benthic nitrogen fixation. In: Carpenter EJ, Capone DC (eds) Nitrogen in the marine environment. Academic, New York, pp 105–137

    Google Scholar 

  • Capone DG, Carpenter EJ (1999) Nitrogen fixation by marine cyanobacteria: historical and global perspectives. In: Charpy L, Larkum AWD (eds) Marine cyanobacteria. Muséé Océanographic, Monaco, pp 235–256

    Google Scholar 

  • Capone DG, Dunham SE, Horrigan SG, Duguay LE (1992) Microbial nitrogen transformations in unconsolidated coral reef sediments. Mar Ecol Prog Ser 80:75–88

    Article  CAS  Google Scholar 

  • Carpenter EJ, Van Raalte CD, Valiela I (1978) Nitrogen fixation by algae in a Massachusetts salt marsh. Limnol Oceanogr 23:318–327

    CAS  Google Scholar 

  • Charpy-Roubaud C, Charpy L, Larkum AW (2001) Atmospheric dinitrogen as a source of nitrogen for the primary benthic production of Tikehau Lagoon (Tuamotu Archipelago, French Polynesia). Mar Biol 139:991–997

    Article  CAS  Google Scholar 

  • Defarge C, Trichet J, Maurin A, Hucher M (1994) Kopara in polynesian atolls: early stages of formation of calcareous stromatolites. Sediment Geol 89:9–23

    Article  CAS  Google Scholar 

  • D’Elia CF (1988) The cycling of essential elements in coral reefs. In: Pomeroy LR, Alberts JJ (eds) Concepts of ecosystem ecology. Springer, Berlin Heidelberg New York, pp 195–230

    Google Scholar 

  • D’Elia CF, Wiebe WJ (1990) Biogeochemical nutrient cycles in coral-reef ecosystems. In: Dubinski Z (ed) Coral reefs. Elsevier, London, pp 49–74

    Google Scholar 

  • Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56:340–373

    PubMed  CAS  Google Scholar 

  • Flett RJ, Hamilton RD, Campbell NER (1976) Aquatic acetylene—reduction techniques: solutions to several problems. Can J Microbiol 22:43–51

    Article  PubMed  CAS  Google Scholar 

  • Gallon JR, Stal LJ (1992) N2 fixation in non-heterocystous cyanobacteria: an overview. In: Carpenter EJ, Capone DG, Reuter JG (eds) Marine pelagic cyanobacteria: Trichodesmium and other diazotrophs. Kluwer, London, pp 115–140

    Google Scholar 

  • Guerinot ML, Colwell RR (1985) Enumeration, isolation, and characterization of N2-fixing bacteria from seawater. Appl Environ Microbiol 50:350–355

    PubMed  CAS  Google Scholar 

  • Guerrero R, Mas J (1989) Multilayered microbial communities in aquatic ecosystems: growth and loss factors. In: Cohen Y, Rosenberg E (eds) Microbial mats, physiological ecology of benthic microbial communities, pp 37–51

  • Hanson RB (1974) Biological nitrogen fixation in a subtropical eutrophic estuary of Kanehoe Bay, Oahu, Hawaii. PhD Dissertation, University Hawaii

  • Haselkorn R (1986) Organization of the genes for nitrogen fixation in photosynthetic bacteria and cyanobacteria. Annu Rev Microbiol 40:525–547

    Article  PubMed  CAS  Google Scholar 

  • Intes A, Caillart B (1994) Environment and biota of the Tikehau Atoll (Tuomotu) Archipelago, French Polynesia. Atoll Res Bull 415:1–34

    Google Scholar 

  • Joye SB, Paerl HW (1994) Nitrogen cycling in microbial mats: rates and patterns of denitrification and nitrogen fixation. Mar Biol 119:285–295

    Article  CAS  Google Scholar 

  • Kamees HS, Gallon JR, Chaplin AE (1987) The pattern of acetylene reduction by cyanobacteria grown under alternating light and darkness. Br Phycol J 22:55–60

    Article  Google Scholar 

  • Larkum AWD (1988) High rates of nitrogen fixation on coral skeletons after predation by the crown of thorns starfish Acanthaster planci. Mar Biol 97:503–506

    Article  CAS  Google Scholar 

  • Larkum AWD, Kennedy IR, Muller WJ (1988) Nitrogen fixation on a coral reef. Mar Biol 98:143–155

    Article  Google Scholar 

  • Lenhardt X (1991) Hydrodynamique des lagons d’atoll et îles hautes en Polynésie Française. Edition de l’ORSTOM. Etudes et Thèses, Paris

  • Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000

    Article  PubMed  CAS  Google Scholar 

  • Lewis JB (1977) Processes of organic production on coral reefs. Biol Rev 52:305–347

    Article  CAS  Google Scholar 

  • Lundgren P, Bauer K, Lugomela, Soderback E, Bergman B (2003) Reevaluation of the nitrogen fixation behavior in the marine non-heterocystous cyanobacterium Lyngbya majuscula. J Phycol 39:310–314

    Article  CAS  Google Scholar 

  • Mague TH, Holm-Hansen O (1975) Nitrogen fixation on a coral reef. Phycologia 14:87–92

    Google Scholar 

  • O’Neil JM, Capone DG (1989) Nitrogenase activity in tropical carbonate marine sediments. Mar Ecol Prog Ser 56:145–156

    Article  CAS  Google Scholar 

  • Paerl HW (1990) Physiological ecology and regulation of N2 fixation in natural waters. Adv Microb Ecol 11:305–344

    CAS  Google Scholar 

  • Paerl HW, Bland (1982) Localized tetrazolium reduction in relation to N2 fixation, CO2 fixation and H2 uptake in aquatic filamentous cyanobacteria. Appl Environ Microbiol 43:218–226

    PubMed  CAS  Google Scholar 

  • Paerl HW, Pinckney JL (1996) A minireview of microbial consortia—their roles in aquatic production and biogeochemical cycling. Microbial Ecol 31:225–247

    Article  Google Scholar 

  • Paerl HW, Zehr T (2000) Nitrogen fixation. In: Kirchman D (ed) Microbial ecology of the oceans. Academic, New York, pp 387–426

    Google Scholar 

  • Paling EI, McComb AJ, Pate JS (1989) Nitrogen fixation (acetylene reduction) in non-heterocystous cyanobacterial mats from the Dampier Archipelago, Western Australia. Aust J Mar Freshwater Res 40:147–153

    Article  CAS  Google Scholar 

  • Pearson HW, Howsley R, Kjeldsen CK, Walsby AE (1979) Aerobic nitrogenase activity associated with a non-heterocystous filamentous cyanobacterium. FEMS Microbiol Lett 5:163–167

    Article  CAS  Google Scholar 

  • Postgate JR (1982) The fundamentals of nitrogen fixation. Cambridge University Press, New York

    Google Scholar 

  • Potts M, Whitton BA (1977) Nitrogen fixation by blue-green algal communities in the intertidal zone of the Lagoon of Aldaba Atoll. Oecologia 27:275–283

    Article  Google Scholar 

  • Ryther JH, Dunstan WM (1971) Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science 171:1008–1013

    Article  PubMed  CAS  Google Scholar 

  • Seitzinger SP, Garber JH (1987) Nitrogen fixation and 15N2 calibration of the acetylene reduction assay in coastal marine sediments. Mar Ecol Prog Ser 37:65–73

    Article  CAS  Google Scholar 

  • Shashar N, Feldstein T, Cohen Y, Loya Y (1994) Nitrogen fixation (acetylene reduction) on a coral reef. Coral Reefs 13:171–174

    Article  Google Scholar 

  • Shilo M (1989) The unique characteristics of benthic cyanobacteria. In: Cohen Y, Rosenberg E (eds) Microbial mats. Physiological ecology of benthic microbial communities, pp 207–213

  • Skyring GW, Lynch RM, Smith GD (1988) Acetylene reduction and hydrogen metabolism by a cyanobacterial/sulfate-reducing bacterial mat ecosystem. Geomicrobiol J 6:25–31

    Article  CAS  Google Scholar 

  • Slawyk G, Raimbault P (1995) Simple procedure for simultaneous recovery of dissolved inorganic and organic nitrogen in 15N-tracer experiments and improving the isotopic mass balance. Mar Ecol Prog Ser 124:289–299

    Article  CAS  Google Scholar 

  • Stal LJ, Caumette P (1994) in Microbial mats, NATO-ASI series, vol G 35. Springer, Berlin Heidelberg New York

  • Stal LJ, Grossberger S, Krumbein (1984) Nitrogen fixation associated with the cyanobacterial mat of a marine laminated microbial ecosystem. Mar Biol 82:217–224

    Article  CAS  Google Scholar 

  • Stewart WDP, Fitzgerald GP, Burris RH (1967) In situ studies on N2 fixation using the acetylene reduction technique. Proc Natl Sci USA 58:2017–2078

    Google Scholar 

  • Werner D, Evans HJ, Siedler RJ (1974) Facultatively anaerobic nitrogen-fixing bacteria from the marine environment. Can J Microbiol 20:59–64

    Article  PubMed  CAS  Google Scholar 

  • Whitton BA (1987) Survival and dormancy of blue-green algae. In: Henis Y (ed) Survival and dormancy of microorganisms. Wiley, NewYork, pp 109–167

    Google Scholar 

  • Whitton BA, Potts M (1982) Marine littoral. In: Garr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell, Oxford, pp 515–542

    Google Scholar 

  • Wiebe WJ, Johannes RE, Webb KL (1975) Nitrogen fixation in a coral reef community. Science 188:257–259

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson CR, Williams DM, Sammarco PW, Hogg RW, Trott LA (1984) Rates of nitrogen fixation on coral reefs across the continental shelf on the central Great Barrier Reef. Mar Biol 80:255–262

    Article  CAS  Google Scholar 

  • Williams SL, Carpenter RC (1998) Effects of unidirectional and oscillatory flow on nitrogen fixation (acetylene reduction) in coral reef algal turfs, Kaneohe Bay, Hawaii. J Exp Mar Biol Ecol 226:293–316

    Article  Google Scholar 

Download references

Acknowledgements

This work was carried out in French Polynesia in the framework of the ORSTOM CYEL program and the PNRCO program (France). We thank, T. Le Campion and P. Raimbault for their help with taxonomy and mass-spectrometer analysis, respectively. This work was supported by a grant under the Australia-France Bi-National Science Agreement.

Author information

Authors and Affiliations

  1. IRD, LMI, Université de Provence CESB/ESIL Case 925, 163 Avenue de Luminy, 13288, Marseille Cedex 9, France

    C. Charpy-Roubaud

  2. School of Biological Sciences, University of Sydney, Sydney, NSW, 2006, Australia

    A. W. D. Larkum

Authors
  1. C. Charpy-Roubaud
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. W. D. Larkum
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. W. D. Larkum.

Additional information

Communicated by Environmental Editor B.G. Hatcher

Rights and permissions

Reprints and permissions

About this article

Cite this article

Charpy-Roubaud, C., Larkum, A.W.D. Dinitrogen fixation by exposed communities on the rim of Tikehau atoll (Tuamotu Archipelago, French Polynesia). Coral Reefs 24, 622–628 (2005). https://doi.org/10.1007/s00338-005-0037-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-005-0037-x

Keywords

Search

Navigation