Oceanography The Official Magazine of
The Oceanography Society
Volume 27 Issue 01

View Issue TOC
Volume 27, No. 1
Pages 172 - 183


Eutrophication-Driven Deoxygenation in the Coastal Ocean

By Nancy N. Rabalais , Wei-Jun Cai , Jacob Carstensen, Daniel J. Conley , Brian Fry, Xinping Hu , Zoraida Quiñones-Rivera, Rutger Rosenberg, Caroline P. Slomp, R. Eugene Turner , Maren Voss, Björn Wissel , and Jing Zhang 
Jump to
Article Abstract Citation References Copyright & Usage
Article Abstract

Human activities, especially increased nutrient loads that set in motion a cascading chain of events related to eutrophication, accelerate development of hypoxia (lower oxygen concentration) in many areas of the world’s coastal ocean. Climate changes and extreme weather events may modify hypoxia. Organismal and fisheries effects are at the heart of the coastal hypoxia issue, but more subtle regime shifts and trophic interactions are also cause for concern. The chemical milieu associated with declining dissolved oxygen concentrations affects the biogeochemical cycling of oxygen, carbon, nitrogen, phosphorus, silica, trace metals, and sulfide as observed in water column processes, shifts in sediment biogeochemistry, and increases in carbon, nitrogen, and sulfur, as well as shifts in their stable isotopes, in recently accumulated sediments.


Rabalais, N.N., W.-J. Cai, J. Carstensen, D.J. Conley, B. Fry, X. Hu, Z. Quiñones-Rivera, R. Rosenberg, C.P. Slomp, R.E. Turner, M. Voss, B. Wissel, and J. Zhang. 2014. Eutrophication-driven deoxygenation in the coastal ocean. Oceanography 27(1):172–183, https://doi.org/10.5670/oceanog.2014.21.


Adelson, J.M., G.R. Helz, and C.V. Miller. 2001. Reconstructing the rise of recent coastal anoxia: Molybdenum in Chesapeake Bay sediments. Geochimica et Cosmochimica Acta 65:237–252, https://doi.org/10.1016/S0016-7037(00)00539-1.

Algeo, T.J., and E. Ingall. 2007. Sedimentary Corg : P ratios, paleocean ventilation, and Phanerozoic atmospheric pO2.Palaeogeography, Palaeoclimatology, Palaeoecology 256:130–155, https://doi.org/10.1016/j.palaeo.2007.02.029.

Baden, S.P., L.-O. Loo, L. Pihl, and R. Rosenberg. 1990. Effects of eutrophication on benthic communities including fish: Swedish west coast. Ambio 19:113–122, http://www.jstor.org/stable/4313676.

Baustian, M.M. 2011. Microphytobenthos of the northern Gulf of Mexico hypoxic area and their role in oxygen dynamics. PhD Dissertation, Louisiana State University, Baton Rouge.

Bennett, E.M., S.R. Carpenter, and N.F. Caraco. 2001. Human impact on erodable phosphorus and eutrophication: A global perspective. BioScience 51:227–234, https://doi.org/10.1641/0006-3568(2001)051[0227:HIOEPA]2.0.CO;2.

Brush, G.S. 2009. Historical land use, nitrogen, and coastal eutrophication: A paleoecological perspective. Estuaries and Coasts 32:18–28, https://doi.org/10.1007/s12237-008-9106-z.

Cai, W.-J. 2003. Riverine inorganic carbon flux and rate of biological uptake in the Mississippi River plume. Geophysical Research Letters 30, 1032, https://doi.org/10.1029/2002GL016312.

Cai, W.-J., X. Hu, W.-J. Huang, M.C. Murrell, J.C. Lehrter, S.E. Lohrenz, W.-C. Chou, W. Zhai, J.T. Hollibaugh, Y. Wang, and others. 2011. Acidification of subsurface coastal waters enhanced by eutrophication. Nature Geoscience 4:766–770, https://doi.org/10.1038/ngeo1297.

Chan, F., J. Barth, J. Lubchenco, J. Kirincich, A. Weeks, H. Peterson, W.T. Menge, and B.A. Chan. 2008. Emergence of anoxia in the California Current Large Marine Ecosystem. Science 319:920, https://doi.org/10.1126/science.1149016.

Chen, C.-C., G.-C. Gong, and F.-K. Shiah. 2007. Hypoxia in the East China Sea: One of the largest coastal low-oxygen areas in the world. Marine Environmental Research 64:399–408, https://doi.org/10.1016/j.marenvres.2007.01.007.

Conley, D., S. Björk, E. Bonsdorff, J. Carstensen, G. Destouni, B.G. Gustafsson, S. Hietanen, M. Kortekaas, H. Kuosa, and others. 2009. Hypoxia-related processes in the Baltic Sea. Environmental Science and Technology 43:3,412–3,420, https://doi.org/10.1021/es802762a.

Conley, D.J., J. Carstensen, J. Aigars, P. Axe, E. Bonsdorff, T. Eremina, B.-M. Haahti, C. Humborg, P. Jonsson, J. Kotta, and others. 2011. Hypoxia is increasing in the coastal zone of the Baltic Sea. Environmental Science and Technology 45:6,777–6,783, https://doi.org/10.1021/es201212r.

Conley, D.J., C. Humborg, L. Rahm, O.P. Savchuk, and F. Wulff. 2002. Hypoxia in the Baltic Sea and basin-scale changes in phosphorus biogeochemistry. Environmental Science and Technology 36:5,315–5,320, https://doi.org/10.1021/es025763w.

Cooper, S.R., and G.S. Brush. 1991. Long-term history of Chesapeake Bay anoxia. Science 254:992–996, https://doi.org/10.1126/science.254.5034.992.

Dalsgaard, T., L.D. Brabandere, and P.O.J. Hall. 2013. Denitrification in the water column of the central Baltic Sea. Geochimica et Cosmochimica Acta 106:247–260, https://doi.org/10.1016/j.gca.2012.12.038.

Díaz, R.J., and R. Rosenberg. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321:926–929, https://doi.org/10.1126/science.1156401.

Duarte, C.M., I.E. Hendriks, T.S. Moore, Y.S. Olsen, A. Steckbauer, L. Ramajo, J. Carstensen, J.A. Trotter, and M. McCulloch. 2013. Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuaries and Coasts 36:221–236, https://doi.org/10.1007/s12237-013-9594-3.

Fonselius, S.H. 1969. Hydrography of the Baltic deep basins III. Pp. 1–97 in Series Hydrography Report No. 23, Fishery Board of Sweden, Gothenberg.

Galloway, J.N., A.R. Townsend, J.W. Erisman, M. Bekunda, Z. Cai, J.R. Freney, L. Martinelli, S.P. Seitzinger, and M.A. Sutton. 2008. Transformation of the nitrogen cycle: Recent trends, questions, and potential solutions. Science 320:889–892, https://doi.org/10.1126/science.1136674.

Gilbert, D., N.N. Rabalais, R.J. Díaz, and J. Zhang. 2010. Evidence for greater oxygen depletion rate declines in the coastal ocean than in the open ocean. Biogeosciences 7:2,283–2,296, https://doi.org/10.5194/bg-7-2283-2010.

Gooday, A.J., F. Jorissen, L.A. Levin, J.J. Middelburg, S.W.A. Naqvi, N.N. Rabalais, M. Scranton, and J. Zhang. 2009. Historical records of coastal eutrophication-induced hypoxia. Biogeosciences 6:1–39, https://doi.org/10.5194/bg-6-1707-2009.

Guo, X., W.-J. Cai, W.-J. Huang, Y. Wang, F. Chen, M.C. Murrell, S.E. Lohrenz, L.-Q. Jiang, M. Dai, J. Hartmann, and others. 2012. Carbon dynamics and community production in the Mississippi River plume. Limnology and Oceanography 57:1–17, https://doi.org/10.4319/lo.2012.57.1.0001.

Hagy, J.D., W.R. Boynton, C.W. Keefe, and K.V. Wood. 2004. Hypoxia in Chesapeake Bay, 1950–2001: Long-term change in relation to nutrient loading and river flow. Estuaries 27:634–658, https://doi.org/10.1007/BF02907650.

Hartnett, H., R.G. Keil, J.J. Hedges, and A.H. Devol. 1998. Influence of oxygen exposure time on organic carbon preservation in continental margin sediments. Nature 391:572–574, https://doi.org/10.1038/35351.

Helly, J.J., and L.A. Levin. 2004. Global distribution of naturally occurring marine hypoxia on continental margins. Deep Sea Research Part I 51:1,159–1,168 https://doi.org/10.1016/j.dsr.2004.03.009.

Hofmann, A.F., E.T. Peltzer, P.M. Walz, and P.G. Brewer. 2011. Hypoxia by degrees: Establishing definitions for a changing ocean. Deep-Sea Research Part I 58:1,212–1,226, https://doi.org/10.1016/j.dsr.2011.09.004.

Intergovernmental Panel on Climate Change (IPCC). 2007. Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. M.I. Parry. O.F. Canziani, J.P. Patulikof, P.J. van der Linden, and C.E. Hanson, eds, Cambridge University Press, Cambridge, UK.

IPCC. 2013. Climate Change 2013: The Physical Science Basis. Group I Contribution to the IPCC Fifth Assessment Report, Intergovernmental Panel on Climate Change, Stockholm. Available online at: http://www.ipcc.ch/report/ar5/wg1 (accessed November 18, 2013).

Jäntti, H., and S. Hietanen. 2012. The effects of hypoxia on sediment nitrogen cycling in the Baltic Sea. Ambio 41:161–169, https://doi.org/10.1007/s13280-011-0233-6.

Jilbert, T., and C.P. Slomp. 2013. Rapid high-amplitude variability in Baltic Sea hypoxia during the Holocene. Geology 41:1,183–1,186, https://doi.org/10.1130/G34804.1.

Jilbert, T., C.P. Slomp, B.G. Gustafsson, and W. Boer. 2011. Beyond the Fe-P redox connection: Preferential regeneration of phosphorus from organic matter as a key control on Baltic Sea nutrient cycles. Biogeosciences 8:1,699-1,720, https://doi.org/10.5194/bg-8-1699-2011.

Jørgensen, B.B. 1980. Seasonal oxygen depletion in the bottom waters of a Danish fjord and its effect on the benthic community. Oikos 34:68–76.

Justić, D., T. Legović, and L. Rottini-Sandrini. 1987. Trends in oxygen content 1911–1984 and occurrence of benthic mortality in the northern Adriatic Sea. Estuarine, Coastal and Shelf Science 25:435–445, https://doi.org/10.1016/0272-7714(87)90035-7.

Justić, D., N.N. Rabalais, and R.E. Turner. 1995. Stoichiometric nutrient balance and origin of coastal eutrophication. Marine Pollution Bulletin 30:41–66, https://doi.org/10.1016/0025-326X(94)00105-I.

Karlson, K., R. Rosenberg, and E. Bonsdorff. 2002. Temporal and spatial large-scale effects of eutrophication and oxygen deficiency on benthic fauna in Scandinavian and Baltic waters: A review. Oceanography and Marine Biology Annual Review 40:427–489, https://doi.org/10.1201/9780203180594.ch8.

Keeling, R.F., A. Körtzinger, and N. Gruber. 2010. Ocean deoxygenation in a warming world. Annual Review of Marine Science 2:463–493, https://doi.org/10.1146/annurev.marine.010908.163855.

Levin, L.A. 2003. Oxygen minimum zone benthos: Adaptation and community response to hypoxia. Pp. 1–45 in Oceanography and Marine Biology, An Annual Review, vol. 41. R.N. Gibson and J.A. Atkinson, eds, CRC Press.

Liu, K.-K., L. Atkinson, R. Quiñones, and L. Talaue-McManus. 2010. Carbon and Nutrient Fluxes in Continental Margins: A Global Synthesis. IGBP Book Series, Springer, Berlin, 741 pp.

Middelburg, J., and L.A. Levin. 2009. Coastal hypoxia and sediment biogeochemistry. Biogeosciences 6:1,273–1,293, https://doi.org/10.5194/bg-6-1273-2009.

Milliman, J.D., K.L. Farnsworth, P.D. Jones, K.H. Xu, and L.C. Smith. 2008. Climatic and anthropogenic factors affecting river discharge to the global ocean, 1951–2000. Global and Planetary Change 62:187–194, https://doi.org/10.1016/j.gloplacha.2008.03.001.

Nixon, S.W. 2004. The artificial Nile. American Scientist 94:158–165, https://doi.org/10.1511/2004.2.158.

Parsons, M.L., Q. Dortch, and R.E. Turner. 2002. Sedimentological evidence of an increase in Pseudo-nitzschia (Bacillariophyceae) abundance in response to coastal eutrophication. Limnology and Oceanography 47(2):551–558, https://doi.org/10.4319/lo.2002.47.2.0551.

Pomeroy, L.R., J.E. Sheldon, W.M. Sheldon, J.O. Blanton, J. Amft, and F. Peters. 2000. Seasonal changes in microbial processes in estuarine and continental shelf waters of the south-eastern USA. Estuarine Coastal and Shelf Science 51:415–428, https://doi.org/10.1006/ecss.2000.0690.

Quiñones-Rivera, Z.J., B. Wissel, D. Justić, and B. Fry 2007. Partitioning oxygen sources and sinks in a stratified, eutrophic coastal ecosystem using stable oxygen isotopes. Marine Ecology Progress Series 342:60–83, https://doi.org/10.3354/meps342069.

Quiñones-Rivera, Z.J., B. Wissel, N.N. Rabalais, and D. Justić. 2010. Effects of biological and physical factors on seasonal oxygen dynamics in a stratified, eutrophic coastal ecosystem. Limnology and Oceanography 55:289–304, https://doi.org/10.4319/lo.2010.55.1.0289.

Rabalais, N.N. 2004. Eutrophication. Pp. 819–865 in The Global Coastal Ocean: Multiscale Interdisciplinary Processes. The Sea: Ideas and Observations on Progress in the Study of the Seas, vol. 13. A.R. Robinson, J. McCarthy, and B.J. Rothschild, eds, Harvard University Press, Cambridge, Massachusetts.

Rabalais, N.N., R.J. Díaz, L.A. Levin, R.E. Turner, D. Gilbert, and J. Zhang. 2010. Dynamics and distribution of natural and human-caused coastal hypoxia. Biogeosciences 7:585–619, https://doi.org/10.5194/bg-7-585-2010.

Rabalais, N.N., D.E. Harper Jr., and R.E. Turner. 2001. Responses of nekton and demersal and benthic fauna to decreasing oxygen concentrations. Pp. 115–128 in Coastal Hypoxia: Consequences for Living Resources and Ecosystems Coastal and Estuarine Studies, vol. 58. N.N. Rabalais and R.E. Turner, eds, American Geophysical Union, Washington, DC.

Rabalais, N.N., R.E. Turner, and D. Scavia. 2002. Beyond science into policy: Gulf of Mexico hypoxia and the Mississippi River. BioScience 52:129–142, https://doi.org/10.1641/0006-3568(2002)052[0129:BSIPGO]2.0.CO;2.

Rabalais, N.N., R.E. Turner, B.K. Sen Gupta, D.F. Boesch, P. Chapman, and M.C. Murrell. 2007a. Hypoxia in the northern Gulf of Mexico: Does the science support the Plan to Reduce, Mitigate, and Control Hypoxia? Estuaries and Coasts 30:753–772, https://doi.org/10.1007/BF02841332.

Rabalais, N.N., R.E. Turner, B.K. Sen Gupta, E. Platon, and M.L. Parsons. 2007b. Sediments tell the history of eutrophication and hypoxia in the northern Gulf of Mexico. Ecological Applications 17:S129–S143, https://doi.org/10.1890/06-0644.1.

Tribovillard, N., T.J. Algeo, T. Lyons, and A. Riboulleau. 2006. Trace metals as paleoredox and paleoproductivity proxies: An update. Chemical Geology 232(1–2):12–32, https://doi.org/10.1016/j.chemgeo.2006.02.012.

Turner, R.E., N. Qureshi, N.N. Rabalais, Q. Dortch, D. Justić, R.F. Shaw, and J. Cope. 1998. Fluctuating silicate:nitrate ratios and coastal plankton food webs. Proceedings of the National Academy Sciences of the United States of America 95:13,048–13,051, https://doi.org/10.1073/pnas.95.22.13048.

Turner, R.E., and N.N. Rabalais. 1994. Coastal eutrophication near the Mississippi River delta. Nature 368:619–621, https://doi.org/10.1038/368619a0.

Turner, R.E., and N.N. Rabalais. 2013. Nitrogen and phosphorus phytoplankton growth limitation in the northern Gulf of Mexico. Aquatic Microbial Ecology 68:159–169, https://doi.org/10.3354/ame01607.

Turner, R.E., N.N. Rabalais, R.B. Alexander, G. McIsaac, and R.W. Howarth. 2007. Characterization of nutrient, organic carbon and sediment loads from the Mississippi River into the northern Gulf of Mexico. Estuaries and Coasts 30(5):773–790.

Turner, R.E., N.N. Rabalais, and D. Justić. 2012. Predicting summer hypoxia in the northern Gulf of Mexico: Redux. Marine Pollution Bulletin 64:319–324, https://doi.org/10.1016/j.marpolbul.2011.11.008.

Vaquer-Sunyer, R., and C.M. Duarte. 2008. Thresholds of hypoxia for marine biodiversity. Proceedings of The National Academy of Sciences of the United States of America 105(40):15,452–15,457, https://doi.org/10.1073/pnas.0803833105.

Voss, M., H.W. Bange, J.W. Dippner, J.J. Middelburg, J.P. Montoya, and B. Ward. 2013. The marine nitrogen cycle: Recent discoveries, uncertainties and the potential relevance of climate change. Philosophical Transactions of the Royal Society B 368, https://doi.org/10.1098/rstb.2013.0121.

Wang, X.-C., R.F. Chen, and G.B. Gardner. 2004. Sources and transport of dissolved and particulate organic carbon in the Mississippi River estuary and adjacent coastal waters of the northern Gulf of Mexico. Marine Chemistry 89:241–256, https://doi.org/10.1016/j.marchem.2004.02.014.

Wong, G.T.F., and P.G. Brewer. 1977. The marine chemistry of iodine in anoxic basins. Geochimica et Cosmochimica Acta 41:151–159, https://doi.org/10.1016/0016-7037(77)90195-8.

Zaitsev, Y.P. 1992. Recent changes in the trophic structure of the Black Sea. Fisheries Oceanography 1:180–189, https://doi.org/10.1111/j.1365-2419.1992.tb00036.x.

Zillén, L., D.J. Conley, T. Andrén, E. Andrén, and S. Björck. 2008. Past occurrences of hypoxia in the Baltic Sea and the role of climate variability, environmental change and human impact. Earth-Science Reviews 91:77–92, https://doi.org/10.1016/j.earscirev.2008.10.001.

Copyright & Usage

This is an open access article made available under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution, and reproduction in any medium or format as long as users cite the materials appropriately, provide a link to the Creative Commons license, and indicate the changes that were made to the original content. Images, animations, videos, or other third-party material used in articles are included in the Creative Commons license unless indicated otherwise in a credit line to the material. If the material is not included in the article’s Creative Commons license, users will need to obtain permission directly from the license holder to reproduce the material.