Oceanography > Issues > Archive > Volume 27, Number 1

2014. Oceanography 27(1):184–195, http://dx.doi.org/10.5670/oceanog.2014.22

(Nearly) A Decade of Directly Measured Sediment N2 Fluxes: What Can Narragansett Bay Tell Us About the Global Ocean Nitrogen Budget?

Authors | Abstract | Full Article | Citation | References


Robinson W. Fulweiler | Department of Earth and Environment and Department of Biology, Boston University, Boston, MA, USA

Elise M. Heiss | Department of Earth and Environment, Boston University, Boston, MA, USA



The tight coupling between nitrogen and carbon cycling has important implications for global climate. These two cycles are under growing anthropogenic pressures (e.g., warming temperatures, changes in nitrogen loading). In this article, we use Narragansett Bay as a model system to explore how large- and small-scale human forcings alter marine sediment nitrogen cycling. We measured net sediment N2 fluxes at two stations in Narragansett Bay over a nine-year period (2005–2013), resulting in observed mean net denitrification rates of 85 µmol m–2 h–1 and 40 µmol m–2 h–1 at the highly impacted and the less impacted sites, respectively. However, mean net N-fixation was essentially the same at each site (–89 and –88 µmol m–2 h–1). We found significant relationships between mean summer (June, July, August) water column chlorophyll and mean summer sediment N2 fluxes. Using these relationships and the long-term chlorophyll record in Narragansett Bay, we predicted summer net sediment N2 fluxes for the last 40 years. This approach suggests that the coastal ocean nitrogen cycle responds rapidly to changes in organic matter availability. If such trends hold true for the global ocean, the marine nitrogen cycle as a whole may also be undergoing significant changes.


Full Article

432 KB pdf



Fulweiler, R.W., and E.M. Heiss. 2014. (Nearly) a decade of directly measured sediment N2 fluxes: What can Narragansett Bay tell us about the global ocean nitrogen budget? Oceanography 27(1):184–195, http://dx.doi.org/10.5670/oceanog.2014.22.



Boyce, D.G., M.R. Lewis, and B. Worm. 2010. Global phytoplankton decline over the past century. Nature 466:591–596, http://dx.doi.org/10.1038/nature09268.
Brown, S.M. 2013. Using molecular tools to elucidate controls on microbes driving the nitrogen cycle in marine sediments. PhD dissertation, University of Rhode Island.
Codispoti, L.A. 2007. An oceanic fixed nitrogen sink exceeding 400 Tg Na–1 vs the concept of homeostasis in the fixed-nitrogen inventory. Biogeosciences 4:233–253, http://dx.doi.org/10.5194/bg-4-233-2007.
Codispoti, L.A., J.A. Brandes, J.P. Christensen, A.H. Devol, S.W.A. Naqvi, H.W. Paerl, and T. Yoshinari. 2001. The oceanic fixed nitrogen and nitrous oxide budgets: Moving targets as we enter the Anthropocene? Scientia Marina 65:85–105, http://dx.doi.org/10.3989/scimar.2001.65s285.
Cornwell, J.C., W.M. Kemp, and T.M. Kana. 1999. Denitrification in coastal ecosystems: Methods, environmental controls, and ecosystem level controls, a review. Aquatic Ecology 33:41–54, http://dx.doi.org/10.1023/A:1009921414151.
Dalsgaard, T., B. Thamdrup, and D.E. Canfield. 2005. Anaerobic ammonium oxidation (anammox) in the marine environment. Research in Microbiology 156:457–464, http://dx.doi.org/10.1016/j.resmic.2005.01.011.
Deutsch, C., J.L. Sarmiento, D.M. Sigman, N. Gruber, and J.P. Dunne. 2007. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445:163–167, http://dx.doi.org/10.1038/nature05392.
Eyre, B.D., D.T. Maher, and P. Squire. 2013. Quantity and quality of organic matter (detritus) drives N2 effluxes (net denitrification) across seasons, benthic habitats, and estuaries. Global Biogeochemical Cycles 27, http://dx.doi.org/10.1002/2013GB004631.
Falkowski, P.G. 1997. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387:272–275, http://dx.doi.org/10.1038/387272a0.
Fennel, K., D. Brady, D. DiToro, R.W. Fulweiler, W.S. Gardner, A. Giblin, M.J. McCarthy, A. Rao, S. Seitzinger, M. Thouvenot-Korppoo, and C. Tobias. 2009. Modeling denitrification in aquatic sediments. Biogeochemistry 93:159–178, http://dx.doi.org/10.1007/s10533-008-9270-z.
Fennel, K., J. Wilkin, J. Levin, J. Moisan, J. O’Reilly, and D. Haidvogel. 2006. Nitrogen cycling in the Middle Atlantic Bight: Results from a three-dimensional model and implications for the North Atlantic nitrogen budget. Global Biogeochemical Cycles 20, GB3007, http://dx.doi.org/10.1029/2005GB002456.
Fields, L. 2013. Benthic-pelagic coupling as a function of changing organic inputs in coastal ecosystems. PhD dissertation, Graduate School of Oceanography, University of Rhode Island.
Foster, S.Q. 2012. Response of benthic oxygen consumption, nutrient cycling and net N2-N fluxes to increasing eutrophication: Evidence of change and ecological significance. MS thesis, Department of Earth Sciences, Boston University.
Fulweiler, R.W., S.M. Brown, S.W. Nixon, and B.D. Jenkins. 2013. Evidence and a conceptual model for the co-occurrence of nitrogen fixation and denitrification in heterotrophic marine sediments. Marine Ecology Progress Series 482:57–68, http://dx.doi.org/10.3354/meps10240.
Fulweiler, R.W., and S.W. Nixon. 2012. Net sediment N2 fluxes in a southern New England estuary: Variations in space and time. Biogeochemistry 111:111–124, http://dx.doi.org/10.1007/s10533-011-9660-5.
Fulweiler, R.W., and S.W. Nixon. 2009. Responses of benthic-pelagic coupling to climate change in a temperate estuary. Hydrobiologia 629:147–156, http://dx.doi.org/10.1007/s10750-009-9766-0.
Fulweiler, R.W., S.W. Nixon, and B.A. Buckley. 2010. Spatial and temporal variability of benthic oxygen demand and nutrient regeneration in an anthropogenically impacted New England estuary. Estuaries and Coasts 33:1,377–1,390, http://dx.doi.org/10.1007/s12237-009-9260-y.
Fulweiler, R.W., S.W. Nixon, B.A. Buckley, and S.L. Granger. 2007. Reversal of the net dinitrogen gas flux in coastal marine sediments. Nature 448:180–182, http://dx.doi.org/10.1038/nature05963.
Fulweiler, R.W., S.W. Nixon, B.A. Buckley, and S.L. Granger. 2008. Net sediment N2 fluxes in a coastal marine system: Experimental manipulations and a conceptual model. Ecosystems 11:1,168–1,180, http://dx.doi.org/10.1007/s10021-008-9187-3.
Gardner, W.S., M.J. McCarthy, S. An, D. Sobolev, K.S. Sell, and D. Brock. 2006. Nitrogen fixation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries. Limnology and Oceanography 51:558–568, http://dx.doi.org/10.4319/lo.2006.51.1_part_2.0558.
Gawarkiewicz, G., J. Nelson, R. He, R.W. Fulweiler, J. Goff, T. Grothues, and E. LaBrecque. 2011. Shelf/Slope Processes: Science Opportunities and Issues Relating to the OOI Pioneer Array. OOI/NSF Technical Report, 57 pp.
Graff, J.R., and T.A. Rynearson. 2011. Extraction method influences the recovery of phytoplankton pigments from natural assemblages. Limnology and Oceanography: Methods 9:129–139, http://dx.doi.org/10.4319/lom.2011.9.129.
Gruber, N. 2008. The marine nitrogen cycle: Overview of distributions and processes. Pp. 1–50 in Nitrogen in the Marine Environment, 2nd ed. D.G. Capone, D.A. Bronk, M.R. Mulholland, and E.J. Carpenter, eds, Elsevier, Amsterdam.
Gruber, N., and J.N. Galloway. 2008. An Earth-system perspective of the global nitrogen cycle. Nature 451:293–296, http://dx.doi.org/10.1038/nature06592.
Hamersley, M.R., K.A. Turk, A. Leinweber, N. Gruber, J.P. Zehr, T. Gunderson, and D.G. Capone. 2011. Nitrogen fixation within the water column associated with two hypoxic basins in the Southern California Bight. Aquatic Microbial Ecology 63:193–205, http://dx.doi.org/10.3354/ame01494.
Heiss, E.M., L. Fields, and R.W. Fulweiler. 2012. Directly measured net denitrification rates in offshore New England sediments. Continental Shelf Research 45:78–86, http://dx.doi.org/10.1016/j.csr.2012.06.002.
Johnstone, J. 1908. Conditions of Life in the Sea: A Short Account of Quantitative Marine Biological Research. Cambridge University Press.
Kana, T.M., C. Darkangelo, M.D. Hunt, J.B. Oldham, G.E. Bennett, and J.C. Cornwell. 1994. Membrane inlet mass-spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Analytical Chemistry 66:4,166–4,170, http://dx.doi.org/10.1021/ac00095a009.
Keeling, R.F., A. Kortzinger, and N. Gruber. 2010. Ocean deoxygenation in a warming world. Annual Review of Marine Science 2:199–229, http://dx.doi.org/10.1146/annurev.marine.010908.163855.
Krumholz, J.S. 2012. Spatial and temporal patterns in nutrient standing stock and mass-balance in response to load reductions in a temperate estuary. PhD Dissertation, Graduate School of Oceanography, University of Rhode Island.
Li, Y.Q., and T.J. Smayda. 1998. Temporal variability of chlorophyll in Narragansett Bay, 1973–1990. ICES Journal of Marine Science 55:661–667, http://dx.doi.org/10.1006/jmsc.1998.0383.
Mackas, D.L. 2011. Does blending of chlorophyll data bias temporal trend? Nature 472, E4–E5, http://dx.doi.org/10.1038/nature09951.
McGlathery, K.J., N. Risgaard-Petersen, and P.B. Christensen. 1998. Temporal and spatial variation in nitrogen fixation activity in the eelgrass Zostera marina rhizosphere. Marine Ecology Progress Series 168:245–258, http://dx.doi.org/10.3354/meps168245.
McQuatters-Gollop, A., P.C. Reid, M. Edwards, P.H. Burkill, C. Castellani, S. Batten, W. Gieskes, D. Beare, R.R. Bidigare, E. Head, and others. 2011. Is there a decline in marine phytoplankton? Nature 472, E6–E7, http://dx.doi.org/10.1038/nature09950.
Middelburg, J.J., K. Soetaert, P.M.J. Herman, and C.H.R. Heip. 1996. Denitrification in marine sediments: A model study. Global Biogeochemical Cycles 10:661–673, http://dx.doi.org/10.1029/96GB02562.
Nixon, S.W. 1997. Prehistoric nutrient inputs and productivity in Narragansett Bay. Estuaries 20:253–261, http://dx.doi.org/10.2307/1352341.
Nixon, S.W., B.A. Buckley, S.L. Granger, L.A. Harris, A.J. Oczkowski, R.W. Fulweiler, and L.W. Cole. 2008. Nitrogen and phosphorus inputs to Narragansett Bay: Past, present, and future. Pp. 101–175 in Science for Ecosystem-based Management. A.E. Desbonnet and B.A. Costa-Pierce, eds, Springer, NY.
Nixon, S.W., R.W. Fulweiler, B.A. Buckley, S.L. Granger, B.L. Nowicki, and K.M. Henry. 2009. The impact of changing climate on phenology, productivity, and benthic-pelagic coupling in Narragansett Bay. Estuarine Coastal and Shelf Science 82:1–18, http://dx.doi.org/10.1016/j.ecss.2008.12.016.
Nixon, S.W., S.L. Granger, and B.L. Nowicki. 1995. An assessment of the annual mass balance of carbon, nitrogen, and phosphorus in Narragansett Bay. Biogeochemistry 31:15–61, http://dx.doi.org/10.1007/BF00000805.
Nowicki, B.L. 1991. The fate of nutrient inputs to estuaries: Evidence from estuarine mesocosms. PhD Dissertation, Graduate School of Oceanography, University of Rhode Island.
Nowicki, B.L. 1994. The effect of temperature, oxygen, salinity, and nutrient enrichment on estuarine denitrification rates measured with a modified nitrogen gas flux technique. Estuarine Coastal and Shelf Science 38:137–156, http://dx.doi.org/10.1006/ecss.1994.1009.
Oviatt, C.A. 2004. The changing ecology of temperate coastal waters during a warming trend. Estuaries 27:895–904, http://dx.doi.org/10.1007/BF02803416.
Oviatt, C., A. Keller, and L. Reed. 2002. Annual primary production in Narragansett Bay with no bay-wide winter-spring phytoplankton bloom. Estuarine, Coastal and Shelf Science 54:1,013–1,026, http://dx.doi.org/10.1006/ecss.2001.0872.
Pilson, M.E.Q. 1985. On the residence time of water in Narragansett Bay. Estuaries 8:2–14, http://dx.doi.org/10.2307/1352116.
Rahav, E., B. Herut, N. Stambler, E. Bar-Zeev, M.R. Mulholland, and I. Berman-Frank. 2013. Uncoupling between dinitrogen fixation and primary productivity in the eastern Mediterranean Sea. Journal of Geophysical Research: Biogeosciences 118:195–202, http://dx.doi.org/10.1002/jgrg.20023.
Reichart, G.J., L.J. Lourens, and W.J. Zachariasse. 1998. Temporal variability in the northern Arabian Sea oxygen minimum zone (OMZ) during the last 225,000 years. Paleoceanography 13(6):607–621, http://dx.doi.org/10.1029/98PA02203.
Rykaczewski, R.R., and J.P. Dunne. 2011. A measured look at ocean chlorophyll trends. Nature 472, E5–E6, http://dx.doi.org/10.1038/nature09952.
Seitzinger, S.P. 1982. The importance of denitrification and nitrous oxide production in the nitrogen dynamics and ecology of Narragansett Bay, Rhode Island. PhD Dissertation, Graduate School of Oceanography, University of Rhode Island.
Seitzinger, S.P., and A.E. Giblin. 1996. Estimating denitrification in North Atlantic continental shelf sediments. Biogeochemistry 35:235–260, http://dx.doi.org/10.1007/978-94-009-1776-7_7.
Seitzinger, S., J.A. Harrison, J.K. Bohlke, A.F. Bouwman, R. Lowrance, B. Peterson, C. Tobias, and G. Van Drecht. 2006. Denitrification across landscapes and waterscapes: A synthesis. Ecological Applications 16:2,064–2,090, http://dx.doi.org/10.1890/1051-0761(2006)016[2064:DALAWA]2.0.CO;2.
Seitzinger, S.P., and S.W. Nixon. 1985. Eutrophication and the rate of denitrification and N2O production in coastal marine-sediments. Limnology and Oceanography 30:1,332–1,339, http://dx.doi.org/10.4319/lo.1985.30.6.1332.
Seitzinger, S.P., S.W. Nixon, and M.E.Q. Pilson. 1984. Denitrification and nitrous-oxide production in a coastal marine ecosystem. Limnology and Oceanography 29:73–83.
Smith, L.M. 2011. Impacts of spatial and temporal variation of water column production and respiration on hypoxia in Narragansett Bay. PhD Dissertation, Graduate School of Oceanography, University of Rhode Island.
Vieillard, A.M., and R.W. Fulweiler. 2012. Impacts of long-term fertilization on salt marsh tidal creek benthic nutrient and N2 gas fluxes. Marine Ecology Progress Series 471:11–22, http://dx.doi.org/10.3354/meps10013.