Evolving paradigms and challenges in estuarine and coastal eutrophication dynamics in a culturally and climatically stressed world

Closing Remarks

Synergistic anthropogenic nutrient loading and climatic changes, including warming, enhanced vertical stratification, and periods of increased residence time provides the mechanistic means for accelerating eutrophication and promoting an increase in HAB frequency and intensity in estuarine and coastal waters. Nutrient input reductions are the most obvious “knobs” that can be “tweaked” to reduce estuarine and coastal eutrophication, and as such should be the key component of most management strategies. We have long been aware of the role P inputs play in such a strategy. However, it has become increasingly evident that N input reductions are needed, and in cases that have been examined thoroughly, a dual N and P reduction strategy appears to be the most realistic and effective long-term approach to eutrophication management along the estuarine continuum. A key management priority is to establish N and P input thresholds (e.g., the USEPA’s Total Maximum Daily Loads or TMDLs; the European Union Water Framework Directive- (http://ec.europa.eu/environment/water/index_en.htm)), below which eutrophication and HABs can be controlled in terms of magnitude, temporal and spatial coverage. These thresholds should incorporate the effects of changing hydrologic and temperature conditions, as these factors strongly modulate estuarine and coastal responses to nutrient inputs.

Both the total amounts and ratios of N to P inputs should be considered when developing these thresholds. Ideal input ratios are those that do not favor specific HAB taxa over others, but there does not appear to be a universal ratio- above or below - which HABs can be consistently and reliably controlled (i.e. system-specific input ratios are likely to be most appropriate and effective). Total molar N:P ratios above ~15 may discourage CyanoHAB dominance (cf., Smith and Schindler 2009). However, if the nutrient concentrations in receiving waters of N or P exceed uptake saturation values, a ratio approach for reducing HABs is not likely to be effective.

There are many ways to reduce nutrient inputs on ecosystem-specific scales. Nutrient inputs have been classified as point source and non-point source. Point sources are often associated with well defined and identifiable discharge sites; therefore these nutrient inputs are often considered “low hanging fruit”, i.e., relatively easy to control. It is therefore no surprise to see that most of the short-term successes in nutrient input control are those associated with point sources, including wastewater treatment plant, industrial effluent and other distinct input sources. The major remaining challenge in many watersheds is targeting and controlling nonpoint sources, which frequently are the largest sources of nutrients discharged to coastal waters (National Research Council 2000; US EPA 2011); their controls are likely to play a critical role in mitigating eutrophication and HABs.

Manipulating physical factors that play key roles in controlling the composition and function of phytoplankton (and benthic microalgal) communities will benefit systems sensitive to eutrophication and HABs. Vertical mixing devices, bubblers and other means of breaking down destratification are effective in controlling outbreaks and persistence of some HABs (e.g., cyanobacteria), but only in relatively small systems (cf. Hudnell 2008). Generally, these devices have limitations in estuarine and coastal waters because they simply cannot exert their forces over such large areas and volumes. Furthermore, artificial mixing doesn’t mitigate the underlying problem of nutrient over-enrichment. In fact, this approach may be counterproductive in vertically stratified waters, by transporting bottom water nutrients across the pynocline up to the surface, potentially exacerbating surface-dwelling blooms.

Decreasing water residence time by increasing the flushing rates can reduce or control HABs in these systems (cf. Paerl et al., 2011b). However, care must be taken to make sure that the flushing water is relatively low in nutrient content, to prevent further enrichment, Also, attention must be paid to algal community structuring effects of changing N:P ratios, which can take place as freshwater discharge is altered. Furthermore, few communities can afford to use precious water resources normally reserved for drinking or irrigation water for flushing purposes, especially in regions with limited or drought-impacted freshwater runoff. Lastly, flushing can alter the circulation regimes of estuarine and coastal waters. Therefore, care must be taken to prevent trapping of the HABs in the system by altering the physical environment (e.g., increasing thermal or chemical density stratification, entrainment bays and arms of water bodies), rather than flushing them out of the system.

Nutrient input reductions are in general the most direct, simple, ecologically rational and economically feasible eutrophication and HAB management strategy. Nutrient input reductions aimed specifically at reducing HAB competitive abilities, and possibly combined with physical controls (in systems amenable to those controls), are often the most effective strategies. An obvious strategy, which is gaining traction is applying fertilizers at “agronomic rates”, i.e., satisfying crop needs, while avoiding excesses and modifying drainage ditches and tile drains to increase their efficiency in minimizing nutrient losses (David et al., 2010). Nutrient (specifically N) removal from wastewater can be prohibitively expensive, so that alternative nutrient removal strategies are needed. Alternate strategies may include construction of wetlands, cultivation and stimulation of macrophytes, stocking of herbivorous (specifically cyanobacteria consumers) fish and shellfish species.

In addition to nutrient input reductions, future water management strategies will need to accommodate the hydrological and physical-chemical effects of climatic change.. Without curbing greenhouse gas emissions, future warming trends and hydrological extremeness will degrade estuarine and coastal ecosystem water and habitat quality further, increasing the potential for expansion by opportunistic nuisance microalgae and cyanobacteria.

Acknowledgements

We thank co-workers who assisted with field and laboratory work and manuscript preparation, including B. Abare, J, Braddy, A. Joyner, L. Kelly and R. Sloup. The editorial input from I. Anderson and W. Gardner is much appreciated. This research was funded by the Strategic Environmental Research and Developmental Program (SERDP)-Defense Coastal/Estuarine Research Program, Project SI-1413, The Lower Neuse Basin Association/Neuse River Compliance Association, the North Carolina Dept. of Environment and Natural Resources (ModMon Program), and National Science Foundation Projects OCE 0825466, OCE 0812913, ENG/CBET0826819 and 1230543, and DEB 1119704 and 1240851.

References

Ache, B.W., K.M. Crossett, P.A. Pacheco, J.E. Adkins, and P.C. Wiley. 2013. “The coast” is complicated: a model to consistently describe the nation’s coastal population. Estuaries and Coasts 1–5, DOI: 10.1007/s12237-013-9629-9).

Ahern, K.S., C.R. Ahern, and J.W. Udy. 2007. Nutrient additions generate prolific growth of Lyngbya majuscula (cyanobacteria) in field and bioassay experiments. Harmful Algae 6: 134-151.
Altman, J.C. and H.W. Paerl. 2012. Composition of inorganic and organic nutrient sources influences phytoplankton community structure in the New River Estuary, North Carolina. Aquatic Ecology 42:269-282.
Anderson, I.C., M J. Brush, M.F. Piehler, C.A. Currin, J.W. Stanhope, A.R. Smyth, J.D. Maxey, M.L. Whitehead. 2013. Impacts of Climate-Related Drivers on the Benthic Nutrient Filter in a Shallow Photic Estuary. Estuaries and Coasts DOI 10.1007/s12237-013-9665-5.
Boesch, D.F., E. Burreson, W. Dennison, E. Houde, M. Kemp, V. Kennedy, R. Newell, K. Paynter, R. Orth, and W. Ulanowicz. 2001. Factors in the decline of coastal ecosystems. Science 293: 629-638.

Borsuk, M.E., C.A. Stow, and K.H. Reckhow. 2004. Confounding effect of flow on estuarine response to nitrogen loading. Journal of Environmental Engineering 130: 605-614.

Boynton, W.R. and W.M. Kemp. 1985. Nutrient regeneration and oxygen consumption by sediments along an estuarine salinity gradient. Marine Ecology Progress Series 23: 45-55.
Bricker, S.B., C.G. Clement, D.E. Pirhalla, S.P. Orlando, and D.R.G. Farrow. 1999. National estuarine eutrophication assessment: effects of nutrient enrichment in the Nation’s estuaries. NOAA, National Ocean Service, Special Projects Office, and the National Centers for Coastal Ocean Science, Silver Spring, MD.
Brown, C.A. 1942. "Justus von Liebig--Man and teacher." and "Liebig and the Law of the Minimum"in: Liebig and After Liebig: A century of progress in agricultural chemistry. American Association for the Advancement of Science. The Science Press Printing Co., Lancaster, PA.
Capone, D.G., M. Mulholland, and E. J. Carpenter (Eds.). 2008. Nitrogen in the Marine Environment, Vol. 2. Academic Press, Orlando. FL.
Chai, C, Z. Yu, Z. Shen, X. Song, X. Cao, and Y.Yao. 2009. Nutrient characteristics in the Yangtze River Estuary and the adjacent East China Sea before and after impoundment of the Three Gorges Dam. Science of the Total Environment 407:4687-4695.
Chen C.T.A and F. Millero. 1986. Precise thermodynamic properties for natural waters covering only the limnological range. Limnology and Oceanography 31:657-662.
Cloern, J.E. 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223-253.
Conley, D.J., H.W. Paerl, R.W. Howarth, D.F. Boesch, S.P. Seitzinger, K.E. Havens, C. Lancelot, G.E. Likens. 2009. Controlling eutrophication: Nitrogen and phosphorus. Science 323: 1014-15.
David, M.B., L.E. Drinkwater, and G.F. McIsaac. 2010. Sources of nitrate yields in the Mississippi River Basin. Journal of Environmental Quality 39:1657–1667.
Diaz, R.J. and R. Rosenberg. 2008. Spreading Dead Zones and Consequences for Marine Ecosystems. Science 321: 926-929.
Dortch, Q. and T. E. Whitledge. 1992. Does nitrogen or silicon limit phytoplankton production in the Mississippi River plume and nearby regions? Continental Shelf Research 12: 1293-1309.
Elliott, J.A., S.J. Thackeray, C. Huntingford, R.G. Jones. 2005. Combining a regional climate model with a phytoplankton community model to predict future changes in phytoplankton in lakes. Freshwater Biology 50: 1404-1411.
Elmgren, R., and U. Larsson. 2001. Nitrogen and the Baltic Sea: Managing nitrogen in relation to phosphorus. The Scientific World, Special Edition (S2): 371-377. Balkema Publishers.
Emanuel, K., R. Sundararajan, and J. Williams. 2008. Hurricanes and Global Warming: Results from Downscaling IPCC AR4 Simulations. Bulletin of the American Meteorological Society 89: 347–367.
Ensign, S.H., J.N. Halls, and M.A. Mallin. 2004. Application of digital bathymetry data in an analysis of flushing times of two North Carolina Estuaries. Computers and Geosciences 30: 501–511.
Elser, J.J., M.E.S Bracken, E.E. Cleland, D.S. Gruner, W.S. Harpole, H. Hillebrand, J.T. Bgai, E.W. Seabloom, J.B. Shurin, J.E. Smith. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10: 1124-34.
Feuchtmayr, H., R. Moran, K. Hatton, L. Conner, T. Heyes, B. Moss, I. Harvey, D. Atkinson. 2009. Global warming and eutrophication: effects on water chemistry and autotrophic communities in experimental hypertrophic shallow lake mesocosms. Journal of Applied Ecology 46: 713-723.
Finlay, K., A. Patoine, D.B. Donald, M. Bogard, and P.R. Leavitt. 2010. Experimental evidence that pollution with urea can degrade water quality in phosphorus-rich lakes of the northern Great Plains. Limnology and Oceanography 55: 1213-1230.
Fisher, T.R., A.B. Gustafson, K. Sellner, R. Lacuture, L.W. Haas, R. Magnien, R. Karr, and B. Michael. 1999. Spatial and temporal variation in resource limitation in Chesapeake Bay. Marine Biology 133: 763-778.
Galloway, J.N, E.B. Cowling. 2002. Reactive nitrogen and the world: 200 years of change. Ambio 31: 64-71.
Goldman, C.R. 1981. Lake Tahoe: Two decades of change in a nitrogen deficient oligotrophic lake. Verhandlungen Internationale Vereinigung für Theoretische und Angewandte Limnologie 21: 45-70.
Granéli, E.K., U. Wallström, U. Larsson, and R. Elmgren. 1999. Nutrient limitation of the Baltic Sea area. Ambio 19: 142-151.
Hall, N.S, R.W. Litaker, E. Fensin, J.E. Adolf, A.R. Place, and H.W. Paerl. 2008. Environmental factors contributing to the development and demise of a toxic dinoflagellate (Karlodinium veneficum) bloom in a shallow, eutrophic, lagoonal estuary. Estuaries and Coasts 31: 402-418.
Hall, N.S. and H.W. Paerl. 2011. Vertical migration patterns of phytoflagellates in relation to light and nutrient availability in a shallow, microtidal estuary. Marine Ecology Progress Series 425:1-19.
Hall, N.S., H.W. Paerl, B.L. Peierls, A.C. Whipple, and K.L. Rossignol. 2013. Effects of climatic variability on phytoplankton biomass and community structure in the eutrophic, microtidal, New River Estuary, North Carolina, USA. Estuarine and Coastal Shelf Science 117: 70-82.
Havens, K.E., T. Fukushima, P. Xie, T. Iwakuma, R.T. James, N. Takamura, T. Hanazato, T. Yamamoto. 2001. Nutrient dynamics and the eutrophication of shallow lakes Kasumigaura (Japan), Donghu (PR China), and Okeechobee (USA). Environmental Pollution 111: 262-72.
Howarth, R.W. 1998. An assessment of human influences on inputs of nitrogen to the estuaries and continental shelves of the North Atlantic Ocean. Nutrient Cycling in Agroecosystems 52: 213-223.
Howarth, R.W., R. Marino, J. Lane, J. J. Cole. 1988. Nitrogen fixation rates in freshwater, estuarine, and marine ecosystems. Limnology and Oceanography 33: 669-687.
Howarth, R., D. Anderson, J. Cloem, C. Elfring, C. Hopkinson, B. Lapointe, T. Malone, N. Marcus, K. McGlathery, A. Sharpley, and D. Walker, Nutrient Pollution of Coastal Rivers, Bays, and Seas. 2000. Vol. 7 of Issues in Ecology. Washington, D.C.: Ecological Society of America.
Hudnell, K.H. (Ed.). 2008. Cyanobacterial Harmful Algal Blooms. Springer, London. 950p.
Humborg, C., L. Rahm, D.J. Conley, T. Tamminen, and B. von Bodungen. 2007. Silicon in the Baltic Sea: Long-term Si decrease in the Baltic Sea- A conceivable ecological risk? Journal of Marine Systems 73:221-222.
Jeppesen, E., B. Moss, H. Bennion, L. Carvalho, L. De Meester, H. Feuchtmayr, N. Friberg, M.O. Gessner, M. Hefting, T.L. Lauridsen, et al. 2010. Interaction of climate change and eutrophication. In: Kernan M., Battarbee R.W., Moss B., editors. Climate change impacts on freshwater ecosystems. Chichester (UK): Wiley-Blackwell. p. 119–151.
Jōhnk, K.D., J. Huisman, J. Sharples, B. Sommeijer, P.M. Visser, J.M. Stroom. 2008. Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biology 14, 495-512.
Justić, D., N.N. Rabalais, R.E. Turner and Q. Dortch. 1995. Changes in nutrient structure of river-dominated coastal waters: Stoichiometeric nutrient balance and its consequences. Estuarine, Coastal Shelf Science 40: 339-356.
Kosten, S., V. Huszar, E. Bécares, L. Costa, E. van Donk, L.-A. Hansson, E. Jeppesen, C. Kruk, G. Lacerot, N. Mazzeo, L. De Meester, B. Moss, M. Lurling, T. Noges, S. Romo, M. Scheffer. 2012. Warmer climate boosts cyanobacterial dominance in shallow lakes. Global Change Biology 18:118-126.
Kraberg, A. , N. Wasmund, J. Vanaverbeke, D. Schiedek, K.H. Wiltshire, and N. Mieszkowska. 2011. Regime shifts in the marine environment: Scientific Basis and political context. Marine Pollution Bulletin, 62: 7-20.
Kratzer, C.R. and P.L. Brezonik. 1981. A Carlson-type trophic state index for nitrogen in Florida lakes. Journal of the American Water Resources Association 17: 713–5.

 

Kuffner, I. B. and V. J. Paul. 2001. Effects of nitrate, phosphate and iron on the growth of macroalgae and benthic cyanobacteria from Cocos Lagoon, Guam. Marine Ecology Progress Series 222:63-72.
Laurent, A., K. Fennel, J. Hu, and R. Hetland. 2012. Simulating the effects of phosphorus limitation in the Mississippi and Atchafalaya River plumes. Biogeosciences Discussion 9: 5625–5657.
Lewis, W.M. Jr. and W.A. Wurtsbaugh. 2008. Control of Lacustrine Phytoplankton by nutrients: Erosion of the Phosphorus Paradigm. Internationale Revue gesamten Hydrobiologie 93: 446-65.
Lewis, W.M., W.A. Wurtsbaugh, and H.W. Paerl. 2011. Rationale for control of anthropogenic nitrogen and phosphorus in inland waters. Environmental Science & Technology 45: 10030-10035.
Likens, G.E. (Ed.). 1972. Nutrients and eutrophication. American Society of Limnology and Oceanography, Special Symposium 1. 328 p.
Mallin, M.A., L.B. Cahoon, M.R. McIver, D.C. Parsons and G.C. Shank. 1997. Nutrient limitation and eutrophication potential in the Cape Fear and New River Estuaries. Report No. 313. Water Resources Research Institute of the University of North Carolina, Raleigh, NC.
Mallin, M.A., M.R. McIver, H.A. Wells, D.C. Parsons, and V.L. Johnson. 2005. Reversal of eutrophication following sewage treatment upgrades in the New River Estuary, North Carolina. Estuaries 28: 750–760.
McCarthy, M.J. P.L. Lavrentyev, L. Yang, L. Zhang, Y. Chen, B. Qin, and W.S. Gardner. 2007. Nitrogen dynamics and microbial food web structure during a summer cyanobacterial bloom in a subtropical, shallow, well-mixed, eutrophic lake (Lake Taihu, China). Hydrobiologia 581: 195-207.
Moisander, P.H., L.A. Cheshire, J. Braddy, E.S. Calandrino, M. Hoffman, M.F. Piehler, and H.W. Paerl. 2012. Facultative diazotrophy increases Cylindrospermopsis raciborskii competitiveness under fluctuating nitrogen availability. FEMS Microbiology Ecology 79:800-811.
Moss, B., S. Kosten, M. Meerhoff, R.W. Battarbee, E. Jeppesen, N. Mazzeo, K. Havens, G. Lacerot, Z. Liu, L. De Meester, H. Paerl, and M. Scheffer. 2011. Allied attack: climate change and eutrophication. Inland Waters 1: 101-105.
National Research Council. 2000. Clean Coastal Waters: Understanding and Reducing the Effects of Nutrient Pollution. Ocean Studies Board and Water Science and Technology Board, Commission on Geosciences, Environment, and Resources. National Academy Press, Washington, DC. 405 p.
Naumann, E. 1921. Einige Grundlinien der regionalen Limnologie. Lunds Universitets Årsskrift N.F. II, 17:1–22.
Nixon, S.W. 1995. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41:199-219
Nixon, S.W., J.W. Ammerman, L.P. Atkinson, V.M. Berounski, G. Billen, W.C. Boicourt, W.R. Boynton, T.M. Church, D.M. Ditoro, R. Elmgren, J.H. Garber, A.E. Giblin, R.A. Jahnke, N.J.P. Owens, M.E.Q. Pilson and S.P. Seitzinger. 1996. The fate of nitrogen and phosphorus at the land-sea margin of the North Atlantic Ocean. Biogeochemistry 35: 141-180.
National Oceanic and Atmospheric Administration. 2012. Spatial Trends in Coastal Socioeconomics Demographic Trends Database: 1970-2010. http://coastalsocioeconomics.noaa.gov/
North, R.L., S.J. Guildford, R.E.H. Smith, S.M. Havens, M.R. Twiss. 2007. Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie. Limnology and Oceanography 52: 315-28.
O’Goman, P. 2012. Sensitivity of tropical precipitation extremes to climate change. Nature Geoscience 5: 697–700
Padisak, J., 1997. Cylindrospermopsis raciborskii (Woloszynska) Seenaya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Archiv für Hydrobiologie Supplement 107: 563-593.
Paerl, H.W. 1990. Physiological ecology and regulation of N₂ fixation in natural waters. Advances in Microbial Ecology 11: 305344.
Paerl, H.W. 1997. Coastal eutrophication and harmful algal blooms: Importance of atmospheric deposition and groundwater as “new” nitrogen and other nutrient sources. Limnology and Oceanography 42: 1154-1165.
Paerl, H.W. 2009. Controlling eutrophication along the freshwater–marine continuum: Dual nutrient (N and P) reductions are essential. Estuaries and Coasts 32: 593-601.
Paerl, H.W., M.A. Mallin, C.A. Donahue, M. Go and B.L. Peierls. 1995. Nitrogen loading sources and eutrophication of the Neuse River estuary, NC: Direct and indirect roles of atmospheric deposition. UNC Water Resources Research Institute Report No. 291. 119 p.
Paerl, H.W., J. D. Bales, L.W. Ausley, C.P. Buzzelli, L.B. Crowder, L.A. Eby, J. M. Fear, M. Go, B.L. Peierls, T.L. Richardson and J.S. Ramus. 2001. Ecosystem impacts of 3 sequential hurricanes (Dennis, Floyd and Irene) on the US’s largest lagoonal estuary, Pamlico Sound, NC. Procedings of the National Academy of . Sciences USA. 98(10):5655-5660.
Paerl, H.W., L.M. Valdes, M.F. Piehler, and M.E. Lebo. 2004. Solving problems resulting from solutions: evolution of a dual nutrient management strategy for the eutrophying Neuse River Estuary, North Carolina, USA. Environmental Science and Technology 38: 3068–3073.
Paerl, H.W., L.M. Valdes, J.E, Adolf, B.M. Peierls and L.W. Harding Jr. 2006. Anthropogenic and climatic influences on the eutrophication of large estuarine ecosystems. Limnology and Oceanography 51: 448-462.
Paerl, H.W., L.M. Valdes, A.R. Joyner and V. Winkelmann. 2007. Phytoplankton Indicators of Ecological Change in the Nutrient and Climatically-Impacted Neuse River-Pamlico Sound System, North Carolina. Ecological Applications 17(5): 88-101.
Paerl, H.W. and J. Huisman. 2008. Blooms like it hot. Science 320:57-58.
Paerl, H.W. and M.F. Piehler. 2008. Nitrogen and Marine Eutrophication. pp 529-567, In, D.G, Capone, M. Mulholland and E. Carpenter (Eds.), Nitrogen in the Marine Environment, Vol. 2. Academic Press, Orlando.
Paerl, H.W., J.J. Joyner, A.R. Joyner, K. Arthur, V.J. Paul, J. M. O’Neil, C.A. Heil. 2008. Co-occurrence of dinoflagellate and cyanobacterial harmful algal blooms in southwest Florida coastal waters: a case for dual nutrient (N and P) input controls. Marine Ecology Progress Series 371: 143-153.
Paerl, H.W. and J.T. Scott. 2010. Throwing fuel on the fire: Synergistic effects of excessive nitrogen inputs and global warming on harmful algal blooms. Environmental Science & Technology 44: 7756–7758.
Paerl, H.W., K.L. Rossignol, Nathan S. Hall, B.L. Peierls, and Michael S. Wetz. 2010. Phytoplankton community indicators of short- and long-term ecological change in the anthropogenically and climatically impacted Neuse River Estuary, North Carolina, USA. Estuaries and Coasts 33:485-497.
Paerl, H.W., N.S. Hall and E.S.Calandrino. 2011a. Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Science of the Total Environment 409:1739-1745.
Paerl, H.W., H. Xu, M.J. McCarthy, G. Zhu, B. Qin, Y. Li, and W.S. Gardner. 2011b. Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): The need for a dual nutrient (N & P) management strategy. Water Research 45: 1973-1983.
Paerl, H.W. and D. Justić. 2011. Primary Producers: Phytoplankton Ecology and Trophic Dynamics in Coastal Waters. In: Wolanski, E. and McLusky, D.S. (Eds.) Treatise on Estuarine and Coastal Science, Vol 6, pp. 23–42. Waltham: Academic Press.
Paerl, H.W., and V. Paul. 2011. Climate Change: Links to Global Expansion of Harmful Cyanobacteria. Water Research 46: 1349-1363.
Parma, S. 1980. The history of the eutrophication concept and the eutrophication in the Netherlands. Hydrobiological Bulletin 14:5-11.
Paul, V.J., 2008. Global warming and cyanobacterial harmful algal blooms. In: Hudnell, H.K. (Ed.), Cyanobacterial Harmful Algal Blooms: State of the Science and Research Needs. Advances in Experimental Medicine and Biology, vol. 619. Springer, pp. 239-257.
Peierls, B.L., N.F. Caraco, M.L. Pace, and J.J. Cole. 1991. Human influence on river nitrogen. Nature 350: 386-387.
Peierls, B.L., N.S. Hall and H.W. Paerl. 2012. Non-monotonic responses of phytoplankton biomass accumulation to hydrologic variability: a comparison of two coastal plain North Carolina estuaries. Estuaries and Coasts 35: 1376-1392.
Peeters, J.C.H., and L. Peperzak. 1990. Nutrient limitation in the North Sea: A bioassay approach. Netherlands Journal of Sea Research 26: 61-73.
Rabalais, N.N. 2002. Nitrogen in aquatic ecosystems. Ambio16: 102-12.
Rabalais, N.N, and R.E. Turner (Eds.). 2001. Coastal Hypoxia: Consequences for Living resources and Ecosystems. Coastal and Estuarine Studies 58. American Geophysical Union, Washington, DC. 454p.
Redfield, A.C. 1958. The biological control of chemical factors in the environment. American Scientist 46: 205-222.
Redfield, A.C., B.H. Ketchum, and F.A. Richards. 1963. The influence of organisms on the composition of sea-water. In N.M. Hill (Ed.), The Sea. Wiley-Interscience, New York, 2: 26-77.
Reynolds, C.S. 2006. Ecology of Phytoplankton (Ecology, Biodiversity and Conservation). Cambridge University Press, Cambridge, UK.
Rudek, J., H.W. Paerl, M.A. Mallin, and P.W. Bates. 1991. Seasonal and hydrological control of phytoplankton nutrient limitation in the lower Neuse River Estuary, North Carolina. Marine Ecology Progress Series 75: 133142.
Ryther, J. and W. Dunstan. 1971. Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science 171: 1008-13.
Scheffer, M., D. Straile, E.H. van Nes, H. Hosper. 2001. Climatic warming causes regime shifts in lake food webs. Limnology and Oceanography 46: 1780-1783.
Schindler, D.W. 1975. Wholelake eutrophication experiments with phosphorus, nitrogen and carbon. Verhandlungen Internationale Vereinigung für Theoretische und Angewandte Limnologie 19: 32213231.
Schindler, D.W. 2012. The dilemma of controlling cultural eutrophication of lakes. Proceedings of the Royal Society B doi: 10.1098/rspb.2012.1032.
Schindler, D.W. and J.R. Vallentyne. 2008. The Algal Bowl: Overfertilization of the World's Freshwaters and Estuaries. Univ. of Alberta Press, Edmonton Canada.
Schindler, D.W., R.E. Hecky, D.L. Findlay, M.P. Stainton, B.R. Parker, M. Paterson, K.G. Beaty, M. Lyng, S.E.M. Kasian. 2008. Eutrophication of lakes cannot be controlled by reducing nitrogen input: Results of a 37 year whole ecosystem experiment. Proceedings of the National Academy of Sciences 105: 11254-11258.
Scott, J.T., R.D. Doyle, S.J. Prochnow, and J.D. White. 2008. Are watershed and lacustrine controls on planktonic N₂ fixation hierarchically structured? Ecological Applications 18: 805–819.
Scott, J.T., J.K. Stanley, R.D. Doyle, M.G. Forbes, and B.W. Brooks. 2009. River–reservoir transition zones are nitrogen fixation hot spots regardless of ecosystem trophic state. Hydrobiologia 625:61-68.
Scott, J.T. and M.J. McCarthy. 2010. Nitrogen fixation may not balance the nitrogen pool in lakes over timescales relevant to eutrophication management. Limnology and Oceanography 55: 1265-1270.
Seitzinger, S.P. 1988. Denitrification in freshwater and coastal marine systems: Ecological and geochemical significance. Limnology and Oceanography 33:702-24.
Smith, V.H. and D.W. Schindler. 2009. Eutrophication science: where do we go from here? Trends in Ecology and Evolution 24(4): 201–207.
Spivak, A.C., M.J. Vanni, and E.M. Mette. 2011. Moving on up: can results from simple aquatic mesocosm experiments be applied across broad spatial scales? Freshwater Biology 56: 279-291.
Sprengel, C.P. 1839. Die Lehre vom Dünger oder Beschreibung aller bei der Landwirthschaft gebräuchlicher vegetablilischer, animalischer und mineralischer Düngermaterialien, nebst Erklärung ihrer Wirkungsart. Leipzig.
Sterner, R. 2008. On the phosphorus limitation paradigm for lakes. International Review of Hydrobiology 93: 433-445.
Stüken, A., J. Rücker, T. Endrulat, K. Preussel, M. Hemm, B. Nixdorf, U. Karsten, C. Wiedner. 2006. Distribution of three alien cyanobacterial species (Nostocales) in northeast Germany: Cylindrospermopsis raciborskii, Anabaena bergii and Aphanizomenon aphanizomenoides. Phycologia 45: 696-703.
Suikkanen, S., M. Laamanen, M. Huttunen. 2007. Long-term changes in summer phytoplankton communities of the open northern Baltic Sea. Estuarine and Coastal Shelf Science 71: 580-592.
Sylvan, J.B., Q. Dortch, D.M. Nelson, A.F. Maier Brown, W. Morrison, and J.W. Ammerman. 2006. Phosphorus limits phytoplankton growth on the Louisiana shelf during the period of hypoxia formation. Environmental Science & Technology 40: 7548-7553.
Thienemann, A. 1915. Physikalische und chemische Untersuchungen in den Maaren der Eifel. Verein der preussischen Rheinlande und Westfalens 70:250–302.
Tomas, C.R., J. Peterson, and A.O. Tatters. 2007. Harmful Algal Species from Wilson Bay, New River, North Carolina: Composition, Nutrient Bioassay and HPLC Pigment Analyses. North Carolina Water Resources Research Institute Report number 369. (31 pages). Available at http://repository.lib.ncsu.edu/dr/bitstream/1840.4/2002/1/NC.
Trenberth, K.E. 2005. The impact of climate change and variability on heavy precipitation, floods, and droughts. In Encylopedia of Hydrological Sciences, ed. M.G. Anderson, 1-11. John Wiley and Sons, Hoboken, New Jersey.
US Environmental Protection Agency. 2011. Reactive Nitrogen in the United States: An Analysis of Inputs, Flows, Consequences, and Management Options. Scientific Advisory Board Publication No. EPA-SAB-11-013. Washington, DC.

Washington, DC.

Vitousek, P.M., H.A. Mooney, J. Lubchenko, J.M. Mellilo. 1997. Human domination of Earth’s ecosystem. Science 277: 494-99.
Vollenweider, R A. 1968. Scientific fundamentals of the eutrophication of’ lakes and flowing waters, with particular reference to nitrogen and phosphorus as factors in eutrophication. Organisation for Economic Co-operation and Development, Paris. Technical Report DAS/CS 1/68.27. 250 p.

Watkinson, A.J., J.M. O’Neil, W.C. Dennison. 2005. Ecophysiology of the marine cyanobacterium Lyngbya majuscula (Oscillatoriaceae) in Moreton Bay, Australia. Harmful Algae 4: 697-671.

Webster, P.J., G.J. Holland, J.A. Curry, and H.R. Chang. 2005. Changes in tropical cyclone number, duration, and intensity in a warming environment. Science 309: 1844-1846.
Wetzel, R.G. 2001. Limnology, Third Edition: Lake and River Ecosystems. Academic Press, Orlando, FL.
Wiedner, C., J. Rücker, R. Brüggemann, B. Nixdorf. 2007. Climate change affects timing and size of populations of an invasive cyanobacterium in temperate regions. Oecologia 152: 473-484.
Xu, H., H.W. Paerl, B. Qin, G. Zhu, G. Gao. 2010. Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnology and Oceanography 55: 420-32.
Figure Captions

Figure 1: Conceptual diagram, illustrating the complex interactions of human nutrient inputs, nutrient cycling processes, nutrient limitation (of primary production) characteristics and hydrologic forcing along the freshwater to marine continuum representing estuarine and coastal ecosystems.

Figure 2. Temperature dependence of the specific growth rates of representative species from three eukaryotic phytoplankton classes and of bloom-forming cyanobacterial species common in temperate freshwater and brackish environments. Data points represent a five ^oC moving average of from laboratory growth experiments under light and nutrient-saturated conditions. References for the individual species can be found in Paerl et al. (2011b). Solid lines are a best-fit temperature optimum function (Chen and Millero 1986).
Figure 3. Maps of the (a) New River Estuary and (b) Neuse River Estuary, NC, showing the locations of sampling stations and US Geological Service (USGS) river gaging stations. The USGS gaging station on the Neuse River is located at Fort Barnwell approximately 26 km upstream from New Bern and out of the area covered by panel b.

Figure 4. Dissolved inorganic nitrogen (Fig. 4A) and dissolved inorganic phosphorus (Fig. 4B) loading, as metric tons per day, entering the Neuse River Estuary during years having no major tropical cyclones impacting its watershed (1994) vs. years in which storms (named) impacted the watershed. Note the variability in nutrient loads associated with specific storms, which was largely attributed to the storm tracks relative to the watershed and the amount of rainfall deposited by each storm.

Figure 5. Concentrations and molar ratios of nitrogen and phosphorus versus river flow in the Neuse and New Rivers just above the limit of salt intrusion. River flow and nutrient concentrations were measured at the USGS Gum Branch gaging station for the New River. Neuse River flow was measured at Fort Barnwell and nutrient concentrations were measured at Streets Ferry Bridge.
Figure 6. Impacts of four tropical cyclones on river flow and the downstream distribution of chlorophyll a in the Neuse River Estuary. Dates for each storm represent landfall on the North Carolina coast. Letters above the flow panel correspond with the letters on the chlorophyll a distribution panels. Off-scale chlorophyll a values are written below the peaks. Extremely high flow events, such as the one following Hurricane Floyd (1999), while delivering large amounts of nutrients, also led to “washout” of resident phytoplankton communities, thereby negating the potential stimulatory effect of this event.
Figure 7. Environmental conditions leading to the development of a toxic Karlodinium veneficum bloom in the Neuse River Estuary. A) Neuse River flow at Fort Barnwell, NC showing the runoff pulse from Tropical Storm Ernesto during the fall of 2006. B) Time series of surface (0 m) and bottom (3 m) salinity from automated USGS instrumentation at station CM11, ~ 4 km downstream of station 60 where peak bloom concentrations were observed on 19 October. C) Time series of surface and bottom dissolved inorganic nitrogen at station 60. Inset pie graphs below time series lines show the relative proportion of nitrate (black fill) versus ammonium (white fill) in the DIN pool of surface and bottom waters on 3 October. D) Time series of surface water chlorophyll a, Karlodinium veneficum cell abundance, and flushing time at station 60 (see figure 3 for its location).
Figure 8. Relationship between phytoplankton biomass and flushing time in the New River Estuary, NC from October 2007 through September 2013
Figure 9. Seasonality of picocyanobacteria and raphidophyte blooms in the New River Estuary. Contour plot of zeaxanthin concentration versus time and distance upstream from the New River Inlet with average temperatures from all stations (solid black line, error bars are standard deviation). White circles show the time and spatial locations of raphidophyte blooms defined as chlorophyll a concentrations greater than 40 g L^-1 and raphidophytes comprising more than half of total phytoplankton biovolume.

Directory: pub
pub -> Project Scoring Template Pre-Construction Phase New Core/Branch Campus Projects
pub -> Acm word Template for sig site
pub -> The german unification, 1815-1870
pub -> Baltic Olympiads in Informatics: Challenges for Training Together
pub ->  Preparation of Papers for ieee transactions on medical imaging
pub -> Forthcoming meetings and conferences
pub -> Asilomar Conference on Circuits, Systems & Computers, Pacific Grove, ca, November 1978, pp. 55 58
pub -> Forthcoming meetings and conferences
pub -> Harmonised compatibility and sharing conditions for video pmse in the 7 9 ghz frequency band, taking into account radar use