Why Is Planktonic Nitrogen Fixation So Rare in Coastal Marine Ecosystems? Insights from a Cross-Systems Approach
The process of di-nitrogen (N2) fixation is widespread in nature, including in many aquatic ecosystems. In lakes, N2 fixation by planktonic cyanobacteria often contributes sufficient new nitrogen to maintain phosphorus limitation of primary production. However, it is intriguing that many estuaries and coastal marine ecosystems at salinities greater than 10 ppt are moderately to strongly N-limited despite high nutrient loading, and planktonic N2 fixation is rarely if ever an important process. Here, we review our collaborative research on mechanisms of control of planktonic N2 fixation in lakes and estuaries, using cross-systems and cross-scale comparative approaches. We conclude that a slower gross growth rate of planktonic cyanobacteria in seawater, coupled with a disproportionate sensitivity of heterocystous species to grazing by zooplankton, can severely constrain bloom development and so N2 fixation in estuaries under N-depleted conditions. A slower growth rate in saline vs. freshwaters is in part a consequence of an inhibition of molybdenum uptake by sulfate; the latter is present in much higher concentrations in seawater. Molybdenum is required for N2 fixation using the conventional form of the nitrogenase enzyme. In the chain-forming cyanobacteria that commonly form large blooms under N-depleted conditions in lakes, N2 fixation occurs in heterocysts, which do not produce oxygen from photosynthesis. As such, energy for the N2 fixation process must be supplied by the photosynthetic, vegetative cells. Clipping of filaments by grazing reduces the number of heterocysts that can be supported, and so further limits N2 fixation and population growth when exogenous N is in low supply.
KeywordsNitrogen fixation Molybdenum Nitrogen Estuaries Nutrient limitation
We were fortunate during the development of the ideas and experiments described in the paper to have as colleagues several creative and broad-minded, cross-system comparative ecologists: Jon Cole, Gene Likens, Scott Nixon, and Mike Pace. Francis Chan’s doctoral research was integral to our mesocosm experiments and our understanding of the role of grazing. We thank Norbert Jaworski and others at the EPA Narragansett Bay lab during the 1990s, and Scott Nixon and the members of his lab group at the University of Rhode Island GSO for use of facilities and technical assistance with the mesocosm experiments. Much of the research described here was supported by grants from the NSF Ecosystems Program and an endowment from David R. Atkinson to Cornell University for the support of our research group and salary for RWH.
- Chan F (2001) Ecological controls on estuarine planktonic nitrogen fixation: the roles of grazing and cross-ecosystem patterns in phytoplankton mortality. PhD thesis, Cornell University, Ithaca, NYGoogle Scholar
- Goldman R (1964) Primary productivity and micro-nutrient limiting factors in some North American and New Zealand lakes. Int Ver Theor Angew Limnol Verh 15:365–374Google Scholar
- Howarth RW, Chan F, Marino R (1999) Do top-down and bottom-up controls interact to exclude nitrogen-fixing cyanobacteria from the plankton of estuaries: explorations with a simulation model. Biogeochemistry 46:203–231Google Scholar
- Marino R (2001) An experimental study of the role of phosphorus, molybdenum, and grazing as interacting controls on planktonic nitrogen fixation in estuaries. PhD thesis, Cornell University, Ithaca, NYGoogle Scholar
- Paerl HW, Zehr JP (2000) Nitrogen fixation. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, Inc, Chichester, pp 387–426Google Scholar
- Schaffner WR, Hairston NG Jr, Howarth RW (1994) Feeding rates and filament clipping by crustacean zooplankton consuming cyanobacteria. Verh Internat Verein Limnol 25:2375–2381Google Scholar