Biogeosciences www.biogeosciences.net 1726-4170 1726-4189 6 12 2009 10.5194/bg-6-2935-2009 http://www.biogeosciences.net/6/2935/2009/ http://www.biogeosciences.net/6/2935/2009/bg-6-2935-2009.html http://www.biogeosciences.net/6/2935/2009/bg-6-2935-2009.pdf 2935 2948 2009-12-10 A macro-tidal freshwater ecosystem recovering from hypereutrophication: the Schelde case study T. J. S. Cox tom.cox@ua.ac.be T. Maris K. Soetaert D. J. Conley S. Van Damme P. Meire J. J. Middelburg M. Vos E. Struyf University of Antwerp, Department of Biology, Ecosystem Management research group, Universiteitsplein 1, 2610 Anwerpen, Belgium Netherlands Institute of Ecology (NIOO-KNAW), Centre for Estuarine and Marine Ecology, Korringaweg 7, P.O. Box 140, 4400 AC Yerseke, The Netherlands GeoBiosphere Science Centre, Quaternary Sciences, Sölvegatan 12, 223 62 Lund, Sweden University of Potsdam, Institute of Biochemistry and Biology, Dept. Ecology & Ecosystem Modeling, Am Neuen Palais 10, 14469 Potsdam, Germany We report a 40 year record of eutrophication and hypoxia on an estuarine ecosystem and its recovery from hypereutrophication. After decades of high inorganic nutrient concentrations and recurring anoxia and hypoxia, we observe a paradoxical increase in chlorophyll-<i>a</i> concentrations with decreasing nutrient inputs. We hypothesise that algal growth was inhibited due to hypereutrophication, either by elevated ammonium concentrations, severe hypoxia or the production of harmful substances in such a reduced environment. We study the dynamics of a simple but realistic mathematical model, incorporating the assumption of algal growth inhibition. It shows a high algal biomass, net oxygen production equilibrium with low ammonia inputs, and a low algal biomass, net oxygen consumption equilibrium with high ammonia inputs. At intermediate ammonia inputs it displays two alternative stable states. Although not intentional, the numerical output of this model corresponds to observations, giving extra support for assumption of algal growth inhibition. Due to potential algal growth inhibition, the recovery of hypereutrophied systems towards a classical eutrophied state, will need reduction of waste loads below certain thresholds and will be accompanied by large fluctuations in oxygen concentrations. We conclude that also flow-through systems, heavily influenced by external forcings which partly mask internal system dynamics, can display multiple stable states. Appeltans, W., Hannouti, A., Van~Damme, S., Soetaert, K., Vanthomme, R., Tackx, M., and Meire, P.: Zooplankton in the Schelde estuary (Belgium/The Netherlands). The distribution of Eurytemora affinis: Effect of oxygen?, J. Plankton Res., 25, 1441–1445, 2003. Arndt, S., Vanderborght, J P., and Regnier, P.: Diatom growth response to physical forcing in a macrotidal estuary: Coupling hydrodynamics, sediment transport, and biogeochemistry, J. Geophys. Res., 112, C05045, \doi10.1029/2006JC003581, 2007. Bates, S S., Worms, J., and Smith, J C.: Effects Of Ammonium And Nitrate On Growth And Domoic Acid Production By Nitzschia-Pungens In Batch Culture, Can. J. Fish. Aquat. Sci., 50, 1248–1254, 1993. Billen, G.: Nitrification In Scheldt Estuary – (Belgium And Netherlands), Estuar. Coast. Mar. Sci., 3, 79–89, 1975. Billen, G., Somville, M., Debecker, E., and Servais, P.: A Nitrogen Budget Of The Scheldt Hydrographical Basin, Neth. J. Sea. Res., 19, 223–230, 1985. Billen, G., Lancelot, C., De~Becker, E., and Servais, P.: Modelling microbial processes (phyto- and bacterioplankton) in the Schelde estuary, Hydrobiological Bulletin, 22~pp., 1988. Billen, G., Garnier, J., and Rousseau, V.: Nutrient fluxes and water quality in the drainage network of the Scheldt basin over the last 50 years, Hydrobiologia, 540, 47–67, ECSA Scheldt Estuary, 2005. Carpenter, S., Caraco, N., Correll, D., Howarth, R., Sharpley, A., and Smith, V.: Nonpoint pollution of surface waters with phosphorus and nitrogen, Ecol. Appl., 8, 559–568, 1998. Carpenter, S., Ludwig, D., and Brock, W.: Management of eutrophication for lakes subject to potentially irreversible change, Ecol. Appl., 9, 751–771, 1999. Carpenter, S R., Brock, W A., Cole, J J., Kitchell, J F., and Pace, M L.: Leading indicators of trophic cascades, Ecol. Lett., 11, 128–138, 2008. Cloern, J E.: Our evolving conceptual model of the coastal eutrophication problem, Mar. Ecol.-Prog. Ser., 210, 223–253, 2001. Conley, D J., Carstensen, J., Vaquer-Sunyer, R., and Duarte, C M.: Ecosystem thresholds with hypoxia, Hydrobiologia, 629(1), 21–29, \doi10.1007/s10750-009-9764-2, 2009. Connell, J. and Sousa, W.: On the evidence needed to judge ecological stability or persistence, Am. Nat., 121, 789–824, 1983. de~Bie, M., Starink, M., Boschker, H., Peene, J., and Laanbroek, H.: Nitrification in the Schelde estuary: methodological aspects and factors influencing its activity, FEMS Microbiol Ecol, 42, 99–107, 2002. de~Jong, D. and De~Jonge, V.: Dynamics and distribution of microphytobenthic chlorophyll-a in the Western Scheldt estuary (SW Netherlands), Hydrobiologia, 311, 21–30, 1995. De~Pauw, C.: Bijdrage tot de kennis van milieu en plankton in het Westerschelde-estuarium, Contribution to the knowledge of the environment and plankton in the Westerschelde-estuary, Ph.D. thesis, University of Gent, 1975 (in Dutch). Dent, C., Cumming, G., and Carpenter, S.: Multiple states in river and lake ecosystems, Philos. T. Roy. Soc. B, 357, 635–645, 2002. deYoung, B., Barange, M., Beaugrand, G., Harris, R., Perry, R I., Scheffer, M., and Werner, F.: Regime shifts in marine ecosystems: detection, prediction and management, Trends Ecol. Evol., 23, 402–409, 2008. Diaz, R J. and Rosenberg, R.: Spreading dead zones and consequences for marine ecosystems, Science, 321, 926–929, 2008. Duarte, C M., Conley, D J., Carstensen, J., and Sánchez-Camacho, M.: Return to Neverland: Shifting Baselines Affect Eutrophication Restoration Targets, Estuar. Coast., 32(1), 29–36, 2009. Elliott, M. and McLusky, D S.: The need for definitions in understanding estuaries, Estuar. Coast. Shelf Sci., 55, 815–827, 2002. Frankignoulle, M., Abril, G., Borges, A., Bourge, I., Canon, C., DeLille, B., Libert, E., and Theate, J M.: Carbon dioxide emission from European estuaries, Science, 282, 434–436, 1998. Garnier, J. and Billen, G.: Production vs. Respiration in river systems: An indicator of an "ecological status", Sci. Total. Environ., 375, 110–124, 2007. Gazeau, F., Gattuso, J P., Middelburg, J J., Brion, N., Schiettecatte, L S., Frankignoulle, M., and Borges, A V.: Planktonic and whole system metabolism in a nutrient-rich estuary (the Scheldt estuary), Estuaries, 28, 868–883, 2005. Gong, H., Nilsen, S., and Allen, J.: Photoinhibition of photosynthesis invivo – involvement of multiple sites in a photodamage process under CO₂-free and O₂-free conditions, Biochim. Biophys. Acta, 1142, 115–122, 1993. Gypens, N., Borges, A V., and Lancelot, C.: Effect of eutrophication on air-sea CO2 fluxes in the coastal Southern North Sea: a model study of the past 50 years, Glob. Change Biol., 15, 1040–1056, 2009. Harrison, P J., Yin, K., Lee, J. H W., Gan, J., and Liu, H.: Physical-biological coupling in the Pearl River Estuary, Cont. Shelf Res., 28, 1405–1415, 2008. Heip, C. H R., Goosen, N K., Herman, P. M J., Kromkamp, J., Middelburg, J J., and Soetaert, K.: Production and consumption of biological particles in temperate tidal estuaries, Oceanogr. Mar. Biol., 33, 1–149, 1995. Hofmann, A. F., Soetaert, K., and Middelburg, J. J.: Present nitrogen and carbon dynamics in the Scheldt estuary using a novel 1-D model, Biogeosciences, 5, 981–1006, 2008. Howarth, R., Swaney, D., Butler, T., and Marino, R.: Climatic control on eutrophication of the Hudson River estuary, Ecosystems, 3, 210–215, 2000. Kallqvist, T. and Svenson, A.: Assessment of ammonia toxicity in tests with the microalga, Nephroselmis pyriformis, Chlorophyta, Water. Res., 37, 477–484, 2003. Kemp, W. M., Testa, J. M., Conley, D. J., Gilbert, D., and Hagy, J. D.: Coastal hypoxia responses to remediation, Biogeosciences Discuss., 6, 6889–6948, 2009. Kessler, E.: Hydrogenase, photoreduction and anaerobic growth, in: Algal physiology and biochemistry, edited by: Steward, W., Blackwel scientific publications, Oxford, 456–473, 1974. Krause, G., Koster, S., and Wong, S.: Photoinhibition of photosynthesis under anaerobic conditions studied with leaves and chloroplasts of spinacia-oleracea L., Planta, 165, 430–438, 1985. Kromkamp, J. and Peene, J.: On the possibility of net primary production in the turbid Schelde estuary (SW Netherlands), Mar. Ecol.-Prog. Ser., 121, 249–259, 1995. Kromkamp, J., Peene, J., Vanrijswijk, P., Sandee, A., and Goosen, N.: Nutrients, Light And Primary Production By Phytoplankton And Microphytobenthos In The Eutrophic, Turbid Westerschelde Estuary (The Netherlands), Hydrobiologia, 311, 9–19, 1995. Lancelot, C., Gypens, N., Billen, G., Garnier, J., and Roubeix, V.: Testing an integrated river-ocean mathematical tool for linking marine eutrophication to land use: The Phaeocystis-dominated Belgian coastal zone (Southern North Sea) over the past 50 years, J. Marine Syst., 64, 216–228, 2007. Lancelot, C., Spitz, Y., Gypens, N., Ruddick, K., Becquevort, S., Rousseau, V., Lacroix, G., and Billen, G.: Modelling diatom and Phaeocystis blooms and nutrient cycles in the Southern Bight of the North Sea: the MIRO model, Mar. Ecol.-Prog. Ser., 289, 63–78, 2005. Meire, P., Ysebaert, T., Van~Damme, S., Van~den Bergh, E., Maris, T., and Struyf, E.: The Scheldt estuary: a description of a changing ecosystem, Hydrobiologia, 540, 1–11, 2005. Noppe, H., Ghekiere, A., Verslycke, T., De~Wulf, E., Verheyden, K., Monteyne, E., Polfliet, K., van Caeter, P., Janssen, C R., and De~Brabander, H F.: Distribution and ecotoxicity of chlorotriazines in the Scheldt Estuary (B-NI), Environ. Pollut., 147, 668–676, 2007. Oguz, T. and Gilbert, D.: Abrupt transitions of the top-down controlled Black Sea pelagic ecosystem during 1960–2000: Evidence for regime-shifts under strong fishery exploitation and nutrient enrichment modulated by climate-induced variations, Deep-Sea Res. I, 54, 220–242, 2007. Owens, N.: Estuarine nitrification: a naturally occurring fluidized bed reaction?, Estuar. Coast. Shelf. Sci., 22, 31–44, 1986. Peckol, P. and Rivers, J S.: Physiological responses of the opportunistic macroalgae Cladophora-Vagabunda (L) Vandenhoek and Gracilaria-Tikvahiae (Mclachlan) to environmental disturbances associated with eutrophication, J. Exp. Mar. Biol. Ecol., 190, 1–16, 1995. Petersen, J K., Hansen, J W., Laursen, M B., Clausen, P., Carstensen, J., and Conley, D J.: Regime shift in a coastal marine ecosystem, Ecol. Appl., 18, 497–510, 2008. Regnier, P., Wollast, R., and Steefel, C I.: Long-term fluxes of reactive species in macrotidal estuaries: Estimates from a fully transient, multicomponent reaction-transport model, Mar. Chem., 58, 127–145, 1997. Scheffer, M. and Carpenter, S.: Catastrophic regime shifts in ecosystems: linking theory to observation, Trends Ecol. Evol., 18, 648–656, 2003. Scheffer, M., Carpenter, S., Foley, J A., Folke, C., and Walker, B.: Catastrophic shifts in ecosystems, Nature, 413, 591–596, 2001. Schroder, A., Persson, L., and De~Roos, A.: Direct experimental evidence for alternative stable states: a review, Oikos, 110, 3–19, 2005. Schuchardt, B., Haesloop, U., and Schirmer, M.: The tidal freshwater reach of the Weser estuary: Riverine or estuarine?, Aquat. Ecol., 27, 215–226, 1993. Smith, V H.: Eutrophication of freshwater and coastal marine ecosystems – A global problem, Environ. Sci. Pollut. R., 10, 126–139, 2003. Smith, V H.: Responses of estuarine and coastal marine phytoplankton to nitrogen and phosphorus enrichment, Limnol. Oceanogr., 51, 377–384, 2006. Soetaert, K. and Herman, P.: Carbon flows in the Westerschelde estuary (The Netherlands) evaluated by means of an ecosystem model (MOSES), Hydrobiologia, 311, 247–266, 1995a. Soetaert, K. and Herman, P.: Nitrogen dynamics in the Westerschelde estuary (SW Netherlands) estimated by means of the ecosystem model MOSES, Hydrobiologia, 311, 225–246, 1995b. Soetaert, K. and Herman, P M.: A practical guide to Ecological Modelling. Using R as a Simulation Platform, Springer, 2009. Soetaert, K., Middelburg, J., Heip, C., Meire, P., Van~Damme, S., and Maris, T.: Long-term change in dissolved inorganic nutrients in the heterotrophic Scheldt estuary (Belgium, The Netherlands), Limnol. Oceanogr., 51, 409–423, 2006. Somville, M.: Use Of Nitrifying Activity Measurements For Describing The Effect Of Salinity On Nitrification In The Scheldt Estuary, Appl. Environ. Microb., 47, 424–426, 1984. Strayer, D L., Pace, M L., Caraco, N F., Cole, J J., and Findlay, S. E G.: Hydrology and grazing jointly control a large-river food web, Ecology, 89, 12–18, 2008. Sundby, C. and Schiött, T.: Characterization of the reversible state of photoinhibition occurring in vitro under anaerobic conditions, Photosynth. Res., 33, 195–202, 1992. Tackx, M., Azemar, F., Bouletreau, S., De~Pauw, N., Bakker, K., Sautour, B., Gasparini, S., Soetaert, K., Van~Damme, S., and Meire, P.: Zooplankton in the Schelde estuary, Belgium and the Netherlands: long-term trends in spring populations, Hydrobiologia, 540, 275–278, 2005. Tang, J X., Hoagland, K D., and Siegfried, B D.: Differential toxicity of atrazine to selected freshwater algae, B. Environ. Contam. Tox., 59, 631–637, 1997. Thomas, W H., Hastings, J., and Fujita, M.: Ammonium Input To The Sea Via Large Sewage Outfalls. 2. Effects Of Ammonium On Growth And Photosynthesis Of Southern-California Phytoplankton Cultures, Mar. Environ. Res., 3, 291–296, 1980. Tyystjaervi, E.: Photoinhibition of Photosystem II and photodamage of the oxygen evolving manganese cluster, Coordin. Chem. Rev., 252, 361–376, 2008. Van~Damme, S., Struyf, E., Maris, T., Ysebaert, T., Dehairs, F., Tackx, M., Heip, C., and Meire, P.: Spatial and temporal patterns of water quality along the estuarine salinity gradient of the Scheldt estuary (Belgium and The Netherlands): results of an integrated monitoring approach, Hydrobiologia, 540, 29–45, 2005. Vanderborght, J., Wollast, R., Loijens, M., and Regnier, P.: Application of a transport-reaction model to the estimation of biogas fluxes in the Scheldt estuary, Biogeochemistry, 59, 207–237, 2002. Vanderborght, J P., Folmer, I M., Aguilera, D R., Uhrenholdt, T., and Regnier, P.: Reactive-transport modelling of C,N, and O-2 in a river-estuarine-coastal zone system: Application to the Scheldt estuary, Mar. Chem., 106, 92–110, 2007. Vandijk, G., Vanliere, L., Admiraal, W., Bannink, B., and Cappon, J.: Present State Of The Water-Quality Of European Rivers And Implications For Management, Sci. Total Environ., 145, 187–195, 1994. Wollast, R.: The Scheldt estuary, in: Pollution of the North-Sea: an assessment, edited by: Salomon, W., Bayne, W., Duursma, E., and Forstner, U., Springer-Verlag, Berlin, 183–193, 1988. Wu, R. S S.: Hypoxia: from molecular responses to ecosystem responses, Mar. Pollut. Bull., 45, 35–45, 2002.