Challenges and Opportunities for Science in Reducing Nutrient Over-Enrichment of Coastal Ecosystems

Estuaries Vol. 25, No. 4b, p. 886-900 August 2002

Challenges and Opportunities for Science in Reducing Nutrient Over-enrichment of Coastal Ecosystems

DONALD F. BOESCH*

University of Maryland Center for Environrnental Science, P. O. Box 775, Cambridge, Maryland 21613

ABSTRACT: Nutrient over-enrichment has resulted in major changes in the coastal ecosystems of developed nations in Europe, North America, Asia, and Oceania, mostly taking place over the narrow period of 1960 to 1980. Many estuaries and elnbayments are affected, but the effects of this eutrophication have been also felt over large areas of selni-enclosed seas including the Baltic, North, Adriatic, and Black Seas in Europe, the Gulf of Mexico, and the Seto Inland Sea in Japan. Primary production increased, water clarity decreased, food chains were altered~ oxygen depletion of bottom waters developed or expanded~ seagrass beds were lost~ and harmful algal blooms occurred with increased frequency. This period of dramatic alteration of coastal eeosystems~ mostly for the worse from a human perspeetive~ eoineidedwith the more than doubling of additions of fixed nitrogen to the biosphere from human activities, driven particularly by a more than 5-fold increase in use of manufactured fertilizers during that 20-year period. Nutrient over-enrichment often interacted synergisdcMly with other hunlan activities, such as overfishing, habitat destruction, and other forms of chemical pollution, in contributing to the widespread degradation of coastal ecosystems that was observed during the last half of the 20th century. Science was effective in documenting the consequences and root causes of nutrient over-enrichlnent and has provided the basis for extensive efforts to abate it, ranging from national statutes and regulations to multijurisdictional compacts under the Helsinki Commission for the Baltic Sea~ the Oslo-Paris Commission for the North Sea, and the Chesapeake Bay Program, for example. These efforts have usually been based on a relatively arbitrary goal of reducing nutrient inputs by a certain pereentage~ without much understanding of how and when this would affect the coastal ecosystem. While some of these efforts have succeeded in achieving reductions of inputs of phosphorus and nitrogen, principally through treatment of point-source discharges~ relatively little progress has been made in reducing diffuse sources of nitrogen. Second-generation nlanagenlent goals tend to be based on desired outcomes for the coastal ecosystem and deternlination of the load reductions needed to attain tbenl, for exanlple the Total Daily Maxinlunl Load approach in the U.S. and the Water Franlework Directive in the European Union. Science and technology are now challenged not just to diagllose the degree of eutrophication and its causes, but to contribute to its prognosis and treatment by determining the relative susceptibility of coastal ecosystems to nutrient over-enriehment~ defining desirable and achievable outcomes for rehabilitation efforts, reducing nutrient sources, enhancing nutrient sinks~ strategically targeting these efforts within watersheds, and predicting and observing responses in an adaptive management framework.

Introduction tion by Nixon's definition) that was taking place The infusion of nutrients (particularly nitrogen during the last half of the 20th century. [N] and phosphorus [P]) from the land via runoff Science has done a commendable job of docu- or the deep ocean via upwelling is the reason that menting coastal eutrophication, identifying its root coastal ecosystems are highly productive and sup- causes, and pointing out its actual and potential port most of the world's fisheries. Over a short pe- consequences (Rabalais 2009). As a result, major riod of time during the 1970s and 1980s it was dis- social and political commitments have been mar- covered that large increases in loadings of nutri- shaled in many parts of the world to reduce nutrients fi-om land as a result of human activities were ent over-enrichment. The increased supply of nu- changing many coastal ecosystems around the trients from land is now recognized as one of the world, often for the worse. The rapid growth of most pervasive causes of the degradation of coastal scientific investigation and publication on coastal ecosystems (National Research Council [NRC] over-enrichment (Nixon 1995) was not only a re- 2000). sult of awakening and expansion of research, but Although it was not necessarily easy for the sci- also of the concomitant rapid increase in the sup- entists engaged in this transition, the path and rec- ply of organic matter in the water bodies stimulat- ognition of the problem through commitment to ed by the increased nutrient loading (eutrophica- alleviate it happened quite quickly in the course of human events. When I moved from the Chesa- * Corresponding author; tele: 410/228-9250; fax: 410/228- peake Bay region in 1980, debates were unresolved 3843; e-mail: [email protected]. about the effects of nutrient over-enrichment on

2002 Estuarine Research Federation 886 Science and Reducing Over-enrichment 887

the bay as a whole and whether N was at all a factor. Subject to light limitation, the greater availability When I returned to the region in 1990, I found a of N and P increases primary production of phy- large intergovernmental establishment pursuing a toplankton and, in some cases, benthic macroalgae nearly single-minded goal of reducing both N and or macrophytes. The resulting increase in phyto- P inputs by 40% by the year 9000. While working plankton biomass commonly reduces water clarity on the Gulf of Mexico coast I helped initiate a re- and results in greater delivery of organic matter to search program with Nancy Rabalais and Gene bottom waters and the seabed. Nutrient enrich- Turner in 1985 on the scope and causes of hypoxia ment also results in qualitative changes in the dom- on the Louisiana inner continental shelf. To say inant primary producers, both in the water column that our hypothesis that hypoxia was linked to in- and photic zone benthic environments. This may creased loadings of nutrients from the Mississippi cause intense blooms, including harmful algal River was greeted with skepticism by agencies and blooms that produce toxins or nuisance condi- regional scientists alike is putting it mildly. It is just tions. Increased organic production and nutrient a natural phenomenon we were told and, besides, supply also stimulate microbial populations and it would never be politically possible to reduce nu- processes, making the microbial loop a more trient inputs in the heartland of American agricul- prominent trophic pathway. tural production, so far away from the Guls Fifteen The enhanced organic production may result in years later, eight federal agencies, nine states, and increased secondary production that extends two tribal governments agreed to a plan to reduce through food chains to exploited fishery popula- the extent of hypoxia to a level that would proba- tions, particularly of pelagic species (Caddy 1998, bly require reduction of upstream N inputs by 30% 2000), but this may not always be the case (Micheli (Rabalais et al. 9002). 1998). On the other hand, decomposition of the So what is next for science? The hard part, really. greater supplies of organic matter often results in Scientists had observations, reconstructions from depletion of dissolved oxygen (hypoxia) in strati- the sediment record, and general theories ground- fied bottom waters to levels too low to sustain fishes ed on experiences elsewhere to develop a convinc- and invertebrates. Diminished water clarity and ing picture of the course of coastal eutrophication. stimulated epiphytic growth may eliminate seagrass As we move into the less traveled territory of de- and microalgal meadows or coral reefs that provide fining achievable states in the rehabilitation of important habitats. Eutrophication that proceeds over-enriched ecosystems, forecasting the trajecto- to the point of producing seasonally persistent hyp- ry of rehabilitation, developing the most effective oxia and extensive loss of shallow vegetated habi- means to reduce nutrient inputs, and observing tats produces obvious negative effects on fishery progress in a highly variable world, scientists will resources. have to be even more resourceful and holistic in their approaches. DISTRIBUTION AND SUSCEPTIBILITY This paper addresses challenges and opportu- These various manifestations of eutrophication nities for science as society moves forward to re- are widely evident in coastal ecosystems of devel- ducing nutrient over-enrichment of coastal ecosys- oped nations, including North America, Europe, tems. I review the nature, scope, and history of Asia, and Australia. They are less well known in the coastal eutrophication, programmatic efforts un- developing world because of lack of study, lower derway to manage the alleviation of nutrient over- loadings of nutrients at their present stage of de- enrichment, and approaches for its abatement. This review sets the stage for the challenges that velopment, or different sensitivities of tropical remain. coastal ecosystems (Corredor et al. 1999). Semi-enclosed seas and large estuaries are affected by hyp- Eutrophication of Coastal Ecosystems oxia, seagrass losses, and algal blooms over sur- prisingly large areas (Fig. 1). This includes deep- ~ANIFESTATIONS basin hypoxia and algal blooms extending over the In his review of evolving concepts of coastal eu- entire southern Baltic Sea (Jansson and Dalhberg trophication, Cloern (2001, p. 226) used the term 1999; Elmgren 2001; Elmgren and Larsson 2001), eutrophication in the sense of "the myriad biogeo- the virtual elimination of the 10,000 km ~ meadow chemical and ecological responses, either direct or of the red alga Phyltophora on the northwestern indirect, to anthropogenic fertilization of ecosys- shelf of the Black Sea (Zaitsev 1999), algal blooms tems at the land-sea interface." These responses and anoxia in the northern Adriatic Sea (Malone can be direct or indirect, acute or chronic, subtle et al. 1999), and a 20,000 km e area of seasonal bot- or profound, and beneficial or detrimental to hu- tom-water hypoxia off the Mississippi and Atchaf- man interests depending on the circumstances. alaya rivers in the northern Gulf of Mexico (Com- BBB D.F. Boesch

AIb em allE- F'a~.,_~alJ~$ a~Baltic Sea ...... $c, und L~n mlcK ~ea nutrient over-enrichment it is important to keep in mind that loadings of both N and P are many-times elevated over background levels for many coastal ecosystems; nutrient limitation varies based on the different biogeochemistry within and between ecosystems and, often, seasonally; and reducing the inputs of one nutrient has consequences for the fate of the other. Phytoplankton production tends to be P-limited in tidal freshwater reaches of estuaries. Reducing P loading to these subsystems can result in increas- Fig. 1. Locations of regions of large-scale nutrient over-en- ing the export of N, not taken up by phytoplank- rictm~ent. ton, to the lower estuarine reaches. Reducing N loading, without reducing P loading, may stimulate N fixation by harmful or noxious cyanobacteria. mittee on Environment and Natural Resources Nutrient limitation can also shift seasonally with P 2000; Rabalais et al. 2002). limitation in spring and N limitation in summer Many smaller bays, estuaries and lagoons in the (Fisher et al. 1999; Conley 2000). Shallow tropical United States (Bricker et al. 1999), Europe (Crouz- ecosystems characterized by carbonate sediments et et al. 1999; Conley et al. 2000), Japan (Suzuki tend to be P rather than N limited (Corredor et 2001), and Australia (McComb 1995) have been al. 1999). Finally, the type of phytoplankton pro- significantly modified by nutrient over-enrichment. duction stimulated is influenced by the ratios of For example, 44 of 1S8 bays and estuaries along available nutrients (Justie et al. 1995), not only of the coast of the U.S. were assessed as having high N and P, but also silicon (which human activities levels of eutrophication and an additional 40 have tend to decrease) and, potentially, other micro- moderate symptoms (Bricker et al. 1999). Fully nutrients or the chemical form of macronutrients 67% of the combined surface area of these bays (e.g., organic N). For all these reasons, it is im- and estuaries exhibit moderate to high degrees of portant that efforts to reduce the deleterious ef- increased phytoplankton growth, increased growth fects of nutrient over-enrichment integrate N and of macroalgae and epiphytes, low dissolved oxygen, P controls rather than just focus on N. harmful algal blooms, and loss of seagrass. It is important to keep in mind that not all coast- EXPLOSIVE INCREASE IN LATE 20TH CENTURY al ecosystems are equally susceptible to nutrient Although human activities have altered the de- over-enrichment. Cloern (9001) contrasts Chesa- livery of nutrients to coastal waters as long as the peake gay, which is particularly sensitive to eutro- human species has been around, these fluxes have phication, with San Francisco gay, which is not. San been successively increased as a result of land clear- Francisco Bay receives higher N and P loading ing for hunting and agriculture, population rates than Chesapeake gay, but has lower standing growth, industrial development, increasing com- stocks of phytoplankton and little or no hypoxia as bustion of fossil fuels, human interest in cleanli- a result of its vigorous tidal mixing and light limi- ness, and the green revolution in agricultural pro- tation caused by sediment resuspension. The rela- duction fueled by mined and manufactured fertil- tive susceptibility of coastal ecosystems depends on izers. The eutrophication of some coastal ecosys- dilution, water residence time and flushing, strati- tems had already advanced by the beginning of the fication, suspended material load or light extinc- 20th century (Conley 9000). The effects of in- tion, among other factors (NRC 9000). This sus- creased delivery of nutrients and sediments that ceptibility can be classified according to the dilu- resulted from agricultural land clearing by Euro- tion and flushing by freshwater inflow and tidal pean colonists are clearly evident in the increased prism volumes (Dettmann 9001) to yield indicators accumulation of organic carbon and biogenic silica that are useful for protection from nutrient over- in Chesapeake Bay sediments (Cooper 1995). In- enrichment. creased deposition of biogenic silica on the Loui- Much attention has been focused on the anthro- siana continental shelf occurred during the 19th pogenic inputs of N as the principal cause of eu- century, also coincident with conversion of land trophication in coastal ecosystems in contrast to within the Mississippi River basin to agriculture freshwater ecosystems, which tend to be P-limited. (Rabalais et al. 1996). The processes that lead to the preponderance of During the early 90th century population N limitation in estuarine and coastal ecosystems growth and industrialization led to intense loading are reviewed by NRC (2000). In efforts to reduce of organic wastes in many coastal ecosystems. The Science and Reducing Over-enrichment 889

TABLE 1. Late 20fl: century manifestations of nutrient over-emictm~ent in major coastal ecosystems in Europe, North America, Japan, and Australia. Except where noted information from Cloern (2001).

O0astal Ecosystem MAI?ifestgtl0 n Period Baltic Sea area Nitrogen supply to Kattegat doubled (Amdersson and Rydberg 1988) 1950-1980 Nitrogen supply to Lanholm Bay tripled (Rosenberg et al. 1990) 1960-1980 Transparency in A_land archipelago decreased by 50% 1984-1994 Primary production in the Kattegat doubled 1960-1980s Area of "dead bottom" in deep Baltic tripled (Jansson and Dahlberg 1999) 1950s--1980s Bottom dissolved oxygen levels in Kattegat decreased by one-fourth 1960s--1980s North Sea and Wadden Sea Nanoplankton biomass at Helgdand tripled (Cdijn and Reise 2001) 1970s--1980s Phytoplankmn biomass and primary production in Wadden Sea doubled 1970-1980 Duration of nondiatom blooms in Wadden Sea increased by tZactor of more than four 1975-1985 Macrobenthos mean w-eight of individual in Wadden Sea decreased by 50% 1970-1980 Macrobenfllos biomass in Wadden Sea doubled 1980-1990 Northern Adriatic Sea PO4 and dissolved inorganic nitrogen concentrations in Po River more than dou- 1970s--1980s bled (Harding et al. 1999) Primary production doubled 1960-1970 Average summer oxygen concentration in bottom layer declined by 37% (Justid et al. 1945-1984 1987) Hypoxia first developed (Justid et al. 1987) 1975 Northwestern Black Sea Inorganic phosphate discharges from Danube River increased 50%, inorganic nitro- 1960-1980s gen discharges increased by factor of 4 (Mee 2001) Transparency decreased by >50% (Zaltsev 1999) 1960s-1970s Phytoplankton biomass increased 40-fold along Romanian coast (Mee 2001) 1963-1985 PhTllopAora algal meadow- decreased by 70% (Zaitsev 1999) 1950s--1980s Large-scale hypoxia first observed (Zaitsev 1999) 1975 Chesapeake Bay NOa in Potomac River inflow- increased 2.5 times (Zimmerman and Canuel 2000) 1960s--1980s Phytoplankmn biomass tripled 1960s--1970s Centric:pennate diatom ratio in sediment record doubled (Cooper 1995) 1950s--1980s Organic carbon incorporation into sedknents increased by 50% (Cornwell et al. 1996) 1960s--1980s Organic enrichment sediment biomarkers increased by factor of three (Zimmerman 1970s--1980s and Canuel 2000) Volume of hypoxic bottom water doubled (Hagy 2002) 1970s--1980s Hypoxia-tolerant benthic Foraminifera doubled in dominance (Karlsen et al. 2000) 1960s-1980s Seagrass extent reduced by 80% (Orth and Moore 1983) 1970-1980 Northern GuK of Mexico Flux of nitrate from Mississippi River Basin tripled 1960s-1980s Incorporation of organic carbon in sediments doubled (Rabalais et al. 1996) 1950s--1980s Incorporation of biogenic silica in sediments doubled (Rabalais et al. 1996) 1960s--1980s Hypoxia-tolerant benthic Foraminifera increased in dominance (Rabalais et al. 1996) 1950s--1980s Tampa Bay Phytoplankmn biomass doubled (Johansson and Greening 2000) 1950s--1970s Seagrass extent reduced by 50% (Johansson and Greening 2000) 1950s--1980s Mikawa Bay Transparency decreased by more than one third (Suzuki 2001) 1960-1970 Days red tides observed tripled (Sukuki 2001) 1970-1983 Seto Inland Sea Number of red tides increased by factor of >4 1960-1975

enrichment effects of organic waste disposal were American and Western Europe (Howarth et al. sometimes severe, but were relatively localized. 1996). Waste treatment to degrade organic matter helped The explosive and synchronous intensification to alleviate these localized effects, such as dissolved of eutrophication in susceptible coastal ecosystems oxygen sags in estuaries (e.g., in the Thames and in North America, Europe, and Japan is striking Delaware Rivers), but did little to reduce the inputs (Table 1). Within two decades (roughly 1960 to of N and P, which are mineralized in the process. 1980), large coastal ecosystems were substantially At the same time, the use of phosphate-based de- changed, as areas of hypoxia developed or greatly tergents compounded the growing eutrophication, intensified, phytoplankton production or biomass particularly in freshwater ecosystems, including the doubled, and benthic macrophyte meadows con- tidal freshwater reaches of estuaries such as the Po- tracted. The coincidence of this period with the tomac River (Jaworski 1990). It was not until after rapid growth of world fertilizer consumption and World War II that the loadings resulting from fossil emission of nitrogen oxides from fossil fuel com- fuel combustion and fertilizer use grew rapidly to bustion is compelling evidence of the primary driv- overwhelm the other sources, causing increases in ing forces of coastal eutrophication (Fig. 2). The river exports of N of 2 to 20 times that of the pre- total N fixed by human activities more than dou- historic levels for coastal regions of eastern North bled between 1960 and 1980 and now probably ex- 890 D.F. Boesch

200 scribes instances where nutrient enrichment from human activities has increased fisheries produc- Period of explosiveincrease -- Totalreactive N ~150 of .... tsl eutrophica~ / tion, particularly of pelagic planktivores. He also pointed out how removal of consumers through 7- / Industriallyfixed fishing may reduce grazing rates and exacerbate ~100~ //(mainly fertilizer) problems related to excess biomass of primary producers (e.g., reduced water clarity, hypoxia). Jack- son et al. (2001) argued for the primacy of over- I~ 50=i _ ~ /~ N-fixingcrops fishing as the cause of the collapse of coastal ecosystems, in the sense that changes related to fishing __ ------'----'-~~ Fossdfuel O ~ combustion preceded other impacts and preconditioned the 1900 1920 1940 1960 1980 2000 susceptibility of ecosystems to these impacts. This seems to be clearly the case for coral reefs and kelp Fig. 9. Period of the explosive increase in coastal eutrophication in relation to global additions of anthropogenically fixed forests among other coastal ecosystems. Human- nitrogen (fixation estimates provided by Galloway, personal enhanced nutrient inputs also began more than a communication). century ago. It is Ulflikely that the eutrophication- related collapses observed in some ecosystems (northwestern shelf of the Black Sea and Gulf of ceeds the total fixed by natural processes in the Mexico, for example) were necessarily precondi- biosphere (Vitousek et al. 1997). The increase in tioned by removal of consumers controlling excess N fertilizer use slowed after 1980 in North Ameri- production from the top down. ca, Europe, and Japan. Most of the global increase Jackson et al. (2001) cited over-harvesting of fil- in fertilizer use after 1980 took place in developing ter feeding oysters in the Chesapeake Bay as setting nations (Tilman et al. 2001). the stage for subsequent changes in that ecosys- Although the nutrient inputs into urbanized tem. It is implausible that restoration of the oyster coastal ecosystems such as Narragansett Bay (Nix- populations alone could completely eliminate the on 1997) and Long Island Sound (Long Island adverse manifestations of nutrient over-enrichment Sound Study 1998) are dominated by municipal without nutrient source reduction. Reducing bot- and industrial waste discharges and atmospheric tom-up nutrient stimulation and increasing top- deposition is a very important source of N in oth- down controls through oyster restoration are, in ers, agriculture is the most important anthropo- fact, both objectives of the Chesapeake restoration gelfiC source of nutrients in inost coastal ecosys- strategy (Boesch et al. 2001b). This exemplifies the tems (Howarth et al. 1996). Controlling agricul- fact that with regard to the management and re- tural inputs of nutrients has been and will remain habilitation of coastal ecosystems, the concept of the most difficult challenge as food production primacy is not very useful. Integrated goals and grows to feed Earth's burgeoning population, pro- strategies are required. jected to stabilize at more than 9 billion during this century (Nixon 1995; Tilman et al. 2001). Managing Coastal Eutrophication It should not be forgotten that humans have al- INSTITUTIONAL ARRANGEMENTS tered coastal ecosystems in many other ways in addition to nutrient over-enrichment. These include Recognition of the impacts of nutrient over-en- massive sedimentation from soil erosion; hydrolog- richment has led to a variety of commitments and ical modification of both catchments and coastal organized efforts to reverse eutrophication and re- environments; the direct (removal of consumers) habilitate the environmental quality and resources and indirect (collateral habitat modification) ef- of degraded coastal ecosystems. These have run fects of fishing; introductions of nonindigenous the gamut from national statutes and regulations species; elimination or modification of habitats, to reduce emissions; multinational directives im- such as wetlands, tidal flats, and oyster reefs, that plemented at the national level; multijurisdictional serve not only as sites of food and refuge but also compacts involving several nations or states, prov- as natural nutrient sinks; and introduction of tox- inces, or prefectures; coastal management pro- icants. Several or all of these maladies have de- grams; and advisory and educational efforts. graded most coastal ecosystems (Elmgren 2001). During the 1970s mounting concerns about en- Furthermore, many of these impacts interact, often vironmental degradation in the semi-enclosed seas synergistically. surrounding Europe led to multinational conven- The interaction of fishing (removing biological tions that have eventually incorporated commit- productivity) and eutrophication (stimulating it) ments for pollution reduction. These are referred deserves particular attention. Caddy (2000) de- to as the Barcelona Convention (1975) for the Science and Reducing Over-enrichment 891

Mediterranean Sea, the Oslo (1972) and Paris The implementation of the commitments under (1974) Conventions for the North Sea, the Helsin- the enclosed seas conventions is left to the signa- ki Convention (1974) for the Baltic Sea, and the tory nations and the level of implementation varies Bucharest Convention (1994) for the Black Sea greatly, especially considering the wide range in (Haas 1990; Crouzet et al. 1999; Mee 2001). Sci- the economic status and governmental capacity of entific and technical assessments are included European nations. Directives adopted by the Eu- among the activities pursuant to each of these con- ropean Union (EU) that are to be implemented ventions. by nations have become a major force for reducing The Barcelona Convention, or Mediterranean nutrient pollution because they are backed by the Action Plan, includes a general commitment to threat of sanctions. This is true even in Eastern take all appropriate measures to prevent, abate, Europe, where nations aspiring to EU membership and combat pollution of the Mediterranean Sea are under pressure to comply with the directives as area, but has not advanced to include many spe- a potential condition for membership (Mee 2001). cific goals for abatement of nutrient pollution These include the Urban Waste Water Treatment (Crouzet et al. 1999). The Oslo Convention, which Directive, which sets minimum standards for the deals with discharges from ships and aircraft, and collection, treatment, and disposal of wastewater the Paris Convention, which addresses land-based dependent on the size of the discharge, and the sources of pollution, were combined in 1992 under type and sensitivity of the receiving waters; the Ni- the Oslo and Paris Commission (OSPAR). In 1987 trate Directive, which aims to reduce or prevent ministers of the OSPAR nations (except for Great the pollution of surface and ground waters caused Britain) set the objective of reducing inputs of N by the application and storage of inorganic fertil- and P by 50% by 1995 into areas where these in- izer and manure on farmland; the Directive on In- puts are likely, directly or indirectly, to cause pol- tegrated Pollution Prevention and Control, which lution. In 1988 the parallel Helsinki Commission is directed to major industries; and the Water (HELCOM) adopted a very similar objective of Framework Directive, which calls for watershed- halving the anthropogenic discharges of N and P based approaches to improve water quality, specific over a 10-year period. goal setting and monitoring and stresses stakehold- The European enclosed coastal sea conventions er involvement (Crouzet et al. 1999; Conley et al. include the littoral states as signatories, e.g., the 9 2002). nations along the shores of the Baltic Sea and the Driven by these multinational conventions and 6 nations bordering the Black Sea. Various efforts EU directives as well as their own domestic con- have also been undertaken to control nutrient in- cerns, some European nations have implemented puts from other non-littoral nations lying within aggressive programs to reduce nutrient pollution the catchments. The catchment area for the Black to coastal waters. Notable among them is Den- Sea, for example, covers nearly 1.7 million km ~ and mark, which has extensive nutrient-impaired estu- includes some 17 nations and 160 million inhabi- aries and coastal waters, intense agriculture, and is tants. These efforts include multinational action party to both the OSPAR and HELCOM conven- plans to reduce nutrient sources in several large tions. In 1986 the Danish Parliament adopted an river basins, i.e., those of the Danube, Rhine and agenda for reducing total loads of N and P to the Elbe Rivers (Crouzet et al. 1999). In 1999 the Is- aquatic environment by 50% and 80%, respective- tanbul Commission for the Bucharest Convention ly, and mandated action plans to achieve these ob- in cooperation with the International Commission jectives (Conley et al. 2002). To direct and track for the Protection of the Danube River recom- progress toward these objectives, the Danish gov- mended that all nations in the Black Sea basin ernrnent operates a substantial National Aquatic should take measures to reduce the loads of nutri- Monitoring and Assessment Program. ents to such levels necessary to permit Black Sea In the U.8. efforts to curtail deleterious nutrient ecosysterns to recover to conditions similar to those inputs to coastal waters began as early as the 1960s observed in the 1960s. These commissions agreed with efforts to control runoff from duck farms into to an intermediate goal that control measures be Moriches Bay on Long Island (Ryther and Dunstan taken by basin states to avoid discharges of nutri- 1971). Abatement of P over-enrichment in fresh ents into the Black Sea exceeding those which ex- waters had been underway for some time in bodies isted in 1997. Because of the collapse of the cen- such as the Great Lakes (U.S. Environmental Pro- trally planned economy in former Communist tection Agency 1995) and P removal from munic- countries and resulting dramatic reduction in fer- ipal Washington, D.C. wastewaters began in the tilizer use, the 1997 nutrient loading levels were 1970s in an effort to improve water quality in the approximately half of those in the late 1980s (Mee tidal Potomac River estuary (Jaworski 1990). Nu- 2001). trient removal was incorporated in treatment of 892 D.F. Boesch

sewage discharges into Tampa Bay beginning in that are party to the regional sea compact which 1980 (Lewis et al. 1998) and eventually resulted in involves only five Gulf coastal states. a 50% reduction in N inputs from these sources. No specific nutrient source reductions are man- The first ambitious effort to effect major reduc- dated under U.S. federal laws but two actions taken tions of both point and diffuse sources of nutrients under the existing Glean Water Act (CWA) are des- over a large region began with the 1987 agreement tined to have an influence on nutrient inputs in among Pennsylvania, Maryland, Virginia, the Dis- U.S. coastal waters. One is the development of nu- trict of Columbia, and the federal government to trient water quality standards by the U.S. Environ- reduce controllable inputs of both N and P into mental Protection Agency (EPA). The other is the the Chesapeake Bay by 40% by the year 2000 court-ordered implementation of a long-neglected (Boesch et al. 2001a). Controllable inputs were provision of the CWA that requires that Total Max- meant to exclude atmospheric sources, runoff imum Daily Loads (TMDLs) of wastes be deter- from forests, and inputs from the three non-sig- mined and allocated through regulatory action if natory states that occupy relatively small portions technology-based standards do not succeed in of the watershed. The Chesapeake Bay Program achieving water quality standards for designated has developed and sustained extensive capabilities uses in water bodies (U.S. EPA 1999; NRC 2000, for assessment, including modeling and monitor- 2001). ing programs, and an expansive implementation Eutrophication of the coastal waters of Japan is structure that have been emulated for other U.S. a particular problem in the major urbanized em- coastal waters included under the National Estuary bayments on the Pacific side of Honshu: Tokyo Program. Bay, Ise Bay (including Mikawa Bay), and the Seto Of the 28 National Estuary Programs, 18 have Inland Sea (including the heavily polluted Osaka identified the impacts of nutrient over-enrichment Bay). In response to worsening water quality and as a high or medium priority for management red tides that interfered with aquaculture activities, (Greening and Elfring 2002) and strategies to re- the Law Concerning Special Measures for Conser- duce nutrient loading are being implemented for vation of the Environment of the Seto Inland Sea 10 of these coastal ecosystems. Management pro- was enacted in 1978. Under the law, the 11 gov- grams for several heavily populated bays and estu- ernors of the prefectures situated around the Seto aries with relatively small catchments rely heavily Inland Sea established administrative guidelines on reduction of point sources of nutrients, either for the reduction of loading of oxygen demanding through advanced waste treatment, such as in Tam- materials and P by 1994. In 1994, N was added to pa and Sarasota Bays and Long Island Sound, or this list. In 1998 the Japanese Environmental Agen- through redirection of these discharges through cy established Environmental Quality Standards deepwater outfalls, such as in Boston Harbor-. A (EQS) and uniform national effluent standards for goal of reducing N loading by 58.5% has been set N and P to reduce marine eutrophication. These for Long Island Sound (Long Island Sound Study effluent standards are effective in the watershed 1998). This is to be met mainly through advanced areas of the 88 designated coastal waters. EQS for treatment of municipal and industrial wastes. For N and P have been applied to Tokyo, Ise, and Osa- Tampa Bay because significant reductions in nutri- ka bays and detailed target reduction figures are ent loading from sewage discharges have already being set for 9004. Point sources in the form of been achieved, the goal is to hold gains made in domestic wastewater and industrial discharges nutrient load reductions by making additional re- dominate nutrient loads in these bays, although ag- ductions in point and diffuse sources to offset the ricultural sources are also important in Ise Bay (Su- effects of anticipated high rate of population zuki 9001) growth in the regron. On a larger scale, in 2000 a task force, working NUTRIENT REDUCTION GOALS under the auspices of the National Science and In the local to regional programs for reducing Technology Council that represented eight federal nutrient over-enrichrnent discussed here, the ini- agencies, nine states, and two tribal governments, tial reduction goals were guided by a combination adopted a general goal of reducing the area ex- of professional judgment and political art. Literally periencing hypoxia in the northern Gulf of Mexico within a few years (1986-1988) goals of 40% to by two-thirds (Rabalais et al. 2002). The task force 50% reduction in nutrient loadings were set for recognized that this would probably require the re- Denmark, OSPAR, the Chesapeake Bay, and HEL- duction of N inputs from the Mississippi River Ba- COM. Crude scientific models and nutrient budget sin by 30%. As in the case of the Black Sea, achieve- reconstructions informed these decisions, but the ment of this goal will depend heavily on actions narrow range of these initial goals suggests that po- taken within jurisdictions beyond the littoral states litical determination of targets that were signifi- Science and Reducing Over-enrichment 893

cantly bold but acceptable by the public also in place to when these affect delivery of nutrients played an important role. These goals were viewed to coastal waters. These lags may be several years as first steps that would achieve significant im- or more, particularly when significant groundwater provements. It was simply important to begin to flows are involved. Finally, it is difficult if not im- reverse the trends. possible to track these changes back to the partic- Once the daunting proportions of these reduc- ular abatement action (e.g., agricultural manage- tions were realized, it was deemed necessary to ment practice or riparian buffer placement) in- qualify what was included in the base to be re- volved. duced and what was not. For the Chesapeake Bay, Efforts to reduce nutrient loadings to coastal the decision was made to exclude background ecosystems are achieving some success. In Den- loadings from forested landscapes, agricultural de- mark, N loads from point sources were reduced by position, and loads from the three nonsignatory 66% and P loads by 81% during the 1990s (Conley states falling partly in the watershed from the re- et al. 2002). Although there were substantial reduction targets. 40% reduction of the remaining ductions of total N and P loadings to Danish coast- controllable sources translated to reductions of al waters, there was not a significant reduction of 91% for total N loading and 36% for total P load- diffuse N loads, which mainly come from agricul- ing (Boesch et al. 2001a). During development of ture. Similar trends in inputs are evident elsewhere action plans based on the 1986 Danish legislation, in Europe, with substantial declines in P loading overall reduction targets changed from being tar- due to reduced use of polyphosphate detergents gets for the total loads to the aquatic environment and treatment of point sources and declines in N to just reduction targets for the losses from agri- loadings where there has been advanced waste culture, municipal waste treatment plants, and sep- treatment of point sources (Crouzet et al. 1999). arate industrial discharges (Conley et al. 9002). Diffuse sources of N, again mainly from agricul- Emissions of N to the atmosphere, storm water ture, seem to have been little reduced. A notable overflows, and P losses from agricultural fields exception is the decline in delivery of N and P to were not included in the targets as implemented. the Black Sea via the Danube River (and probably More recent nutrient reduction goals have been Dniester and Dnieper Rivers) five to seven years set based on simulation models or empirical evi- after the dramatic reduction in fertilizer use that dence. The goal of reducing N loading by 58.5% occurred as a result of the economic changes of for Long Island Sound was developed using hydro- perestroika (Mee 9001). dynamic-water quality modeling to forecast hyp- Modeling procedures are being used to simulate oxic conditions. A level of reduced, but not elimi- progress as well as to forecast future consequences nated, hypoxia was chosen as achieving an accept- for reductions in nutrient loadings on watershed able and attainable level of improvement (Long scales. Abatement actions are credited for certain Island Sound Study 1998). The goal set for the reductions in nutrient loadings, and the changes northern Gulf of Mexico is also based on reduction in the loads delivered to the coastal water are es- of the extent of hypoxia, with a rough model ap- timated as a function of their location on the land- proximation that this would require a 30% reduc- scape and losses during delivery downstream. Such tion of N loading (Rabalais et al. 2002). For the a hydrologic-watershed model is used in the Ches- Black Sea and Tampa Bay the goal is to cap load- apeake Bay Program for both status assessment and ings at levels at which significant reductions of hyp- forecasting (Linker et al. 1996). The model esti- oxia, in the former case, and chlorophyll levels, in mated that abatement actions were in place by the the latter case, had been realized. end of the benchmark year 2000 to result in effective reductions in controllable loadings of 34% for ASSESSING PROGRESS P and 28% for N (31% and 15% of the total loads, Estimation of progress in meeting nutrient re- respectively; Boesch et al. 2001a). In addition to duction goals is a challenge for several reasons. the assumptions regarding the credited loading re- While many point sources can be monitored rea- ductions for the various abatement actions, this as- sonably accurately, diffuse sources are harder to sessment normalizes flow conditions to the 1985 monitor. Nutrient delivery in stream flow may be base year and includes no lag times for watershed highly variable on short time frames, posing esti- delivery. mation problems. Nutrient load is itself strongly A more effective way to track progress in achiev- related to stream flow, which varies greatly among ing goals for reduction of nutrient loading is to years. Procedures for calculation of flow-adjusted combine observations with models, allowing both loadings may be employed to normalize this vari- the assimilation of observational data into the ability (Cohn et al. 1989). Even then, there are models and the identification of sources contrib- time delays from when abatement actions are put uting to changes in observed loadings. Using such B94 D.F. Boesch

an approach, Behrendt (1999) found that N emis- affected coastal waters. The objectives for Danish sions into the North Sea from both the Rhine and marine waters are that the fauna and flora may be Elbe Rivers declined by 29% during the 1990s, and affected only insignificantly or slightly by anthro- that this was mainly due to substantial reductions pogenic pollution, nutrient concentrations have to of municipal and industrial point sources (46%). be at a natural level, the clarity of the water has to The decrease in diffuse inputs was only 10%, again be normal, unnatural blooms of toxic planktonic pointing out the difficulties in reducing agricultur- algae or pollution-dependent macroalgae must not al sources. occur, and oxygen deficiency may only occur in Assessing improvements in the quality of the re- areas where it is natural (Conley et al. 2009). The ceiving coastal waters provides the ultimate test of 2000 Chesapeake Bay Program Agreement does progress. There have yet been few unambiguous not set a specific load reduction goal, but specifies demonstrations of meeting objectives for coastal the objective of correcting nutrient-related prob- ecosystem rehabilitation from over-enrichment. lems needed to remove the bay and its tidal trib- The stepwise reduction of N loading to the Him- utaries from the list of impaired waters under the merfj~rden, on the Baltic coast of Sweden, by 70% CWA (Boesch et al. 2001a). Essentially this means from 1976 to 1998 has resulted in decline in the determining TMDLs to meet water quality stan- concentrations of total N and chlorophyll a that dards for designated uses. The process of deter- approximated forecasts (Elmgren and Larsson mining designated uses and standards, estimating 9001). Reductions in nuisance growth of macroal- the maximum nutrient loads at which those stan- gae, increased water clarity, and reduced phyto- dards can be met, and allocating the maximum ac- plankton production have also been documented ceptable loads among sources is underway not only in Danish coastal waters (Conley et al. 9009). Chlo- for various segments of the Chesapeake Bay but rophyll a levels in Tampa Bay have been reduced also for many other rivers and coastal waters on to a level approximating management goals, but the impaired list. Although not formally based on seagrass recovery has been slower than expected a TMDL, the agreement for N reduction in the (NRC 2000). Mississippi River basin also is based on an environ- In most other areas where nutrient inputs have mental endpoint--reducing the extent of hypoxia been reduced, the trends are mixed or responses (Rabalais et al. 2002). The EU's new Water Framework Directive sets are delayed. In the Chesapeake Bay, statistically sig- up a remarkably parallel process to reconcile the nificant reductions in ambient nutrient concentra- inadequacies of the technology-based emission lim- tions have been observed in some regions where its in achieving environmental quality standards. point source inputs have been reduced but not in The Directive requires river basin scale approaches the open bay or in areas receiving primarily diffuse to defining good ecological status and the stan- source inputs (Boesch et al. 9001a). Trends in ex- dards needed to achieve it, evaluation of the effec- pansion of seagrasses or reduction of hypoxia are tiveness of implementation of existing regulations difficult to decipher from the effects of interan- to achieve these standards, and identification of ad- nual variability of freshwater flows. Delayed re- ditional measures needed to satisfy the objectives sponses due to nutrient storage in the watershed established. New Japanese policies require addi- or coastal system and inherently nonlinear ecosys- tional actions when effluent standards are insuffi- tem responses should be expected. Positive feed- cient to achieve environmental quality standards. backs characterize some of these responses, poten- Such outcome-based approaches as U.S. TMDLs tially resulting in more dramatic improvements and the EU Water Framework Directive present once thresholds are reached. For example, the major new challenges to science and the use of gradual improvement in dissolved oxygen condi- science (NRC 2001). Because returning to a pris- tions should result in increased denitrification and tine state, especially with respect to anthropogenic P burial in bottom sediments (Boesch et al. 2001a). nutrient inputs, is seldom if ever a realistic option, As the Black Sea experiment indicates, responses outcome-based approaches involve the practical in- in the coastal ecos2estem, in this case alleviation of tegration of what is desirable with what is achiev- hypoxia, may lag even dramatic reductions in nu- able. Although in the end these are policy and not trient inputs by as much as a decade (Mee 9001). scientific determinations, science can and should play an integral role in informing the policymak- SECOND-GENERATION GOALS ing process both on desirability and achievability. While load reduction goals based on some practical approximation of outcome served a useful Abatement purpose of mobilizing efforts to reduce nutrient MULTIPRONCED APPROACHES TYPICALLYREQUIRED over-enrichment, new goals are being set to Some coastal waters (bay, estuary, or continental achieve more specific ecological conditions in the shelf region) receive nutrients predominantly from Science and Reducing Over-enrichment 895

one source type (e.g., sewage discharges into Long reduce ground-level ozone that poses human Island Sound), such that a concentrated focus on health risks and stresses forests and crops. Signifi- abatement of nutrient loadings from that source cant reductions in NO X emissions from stationary (e.g., implementing advanced waste treatment) and mobile sources are being mandated to meet would be a sufficient strategy for reducing over- C_&A requirements (U.S. EPA 2000). A 40% reduc- enrichment. Because most over-enriched coastal tion in NOx emissions may ultimately be achieved ecosystems receive loadings from numerous sourc- as a result of new standards, technologies, and ef- es, an integrated strategy for effective abatement is ficiencies being pursued under the C_&A. In Eu- required. The strategy should encompass the rope it is estimated that a 15% reduction in NO x catchment basin, or watershed, draining into the emissions was achieved between 1990 and 1995, al- coastal waters because of the widespread impor- though this was largely due to declines in industrial tance of diffuse sources. It may have to consider activity in Eastern Europe (Crouzet et al. 1999). nutrients originating outside the catchment, but EU directives for reducing industrial emissions and transported into it through the atmosphere. These exhaust emissions from on-road vehicles are ex- are non-conventional units for ocean and coastal pected to result in lowering NOx releases by nearly resource management and pose numerous chal- one-third by 2010. lenges. Abatement of agricultural sources of nutrient Through an integrated strategy substantial re- pollution is proving to be more difficult. To be duction in nutrient loadings to coastal waters may practical, abatement of agricultural sources of nu- be achieved by approaches that reduce the use of trients must focus not only on reducing fertilizer the nutrients in the first place; control losses to the use but also on plugging the many leaks in agri- environment at the point of release (e.g., farm cultural nutrient cycles. Although efficiencies in field, animal feeding operation, lava1 or subdivi- fertilizer use in U.S. agriculture have been slowly sion, vehicle, power plant, or industrial or sewage increasing since the mid-1970s, about one-third of treatment works) ; and sequester or remove pollut- the N applied is not recovered in harvested crops ants (enhance sinks) as they are transported to the (NRC 2000). Not all of the missing N contributes sea. In order to achieve maximum effectiveness of to eutrophication of coastal waters. Much is deni- these interventions at acceptable costs to society trifled in soils or aquatic systems en route to the geographic targeting of source controls and sinks sea or is stored in soils or groundwater. In addition ~s important. to increasing the efficiency of N uptake by crops, the return of N 2 gas to the atmosphere can be en- SOURCES hanced through land management practices. Significant reductions in P loading in Europe, Various agricultural practices affect N and P run- North America, and Japan have resulted from dis- off and losses to groundwater (which ultimately continuing the use of polyphosphate detergents. P seeps into surface waters) or atmosphere. Practices can be almost completely removed from wastewa- employed to reduce soil erosion, such as contour ters by additional chemical and biological treat- plowing, timing of cultivation, conservation tillage ment (NRC 2000). P removal from wastewater in (little or no tilling), stream bank protection, graz- the Washington, D.C. metropolitan area produced ing management, and grassed waterways also re- substantial improvements in water quality and liv- duce nutrient pollution. Other practices are more ing resources in the tidal freshwater portions of the specifically targeted to the efficient use and reten- Potomac estuary, which tend to be P-limited (Ja- tion of nutrients; including soil testing to precisely worski 1990). Advanced wastewater treatment for match fertilizer applications to crop nutritional N removal has reduced point-source N loadings in needs (many farmers still overapply to insure max- Denmark and Sweden. Advanced treatment is be- imum crop yields); applying fertilizer just at the ing applied in Chesapeake, Tampa, and Sarasota time the crop needs it; crop rotation; planting cov- Bays and Long Island Sound employing biological er crops in the fall; using soil and manure amend- nutrient removal, a process that couples microbial ments, and specialized methods of application, nitrification under aerobic conditions with denitri- such as injection (NRC 2000). Reducing the inef- fication under anaerobic conditions (NRC 2000). ficiencies that generally lead to the application of Reductions in nitrogen oxide (NO~) emissions fertilizers in excess of crop requirements can have to the atmosphere have been driven by air quality significant benefits in terms of reducing nutrient considerations generally outside the influence of loadings downstream. For example, using a hind- water quality or coastal ecosystem managers. In the cast, statistical model that adjusted for the effects U.S. NO x emissions from power plants and vehicles of the annual water budget on nitrate flux in the are regulated under the Clean Air Act (CA&); a lower Mississippi River, Mclsaac et al. (2001) esti- key goal of the 1990 Amendments to the act is to mated that a 12% reduction in the application of 896 D.F. Boesch

fertilizers within the river basin could result in a terminous U.S. at the time of European settlement reduction of S3% in nitrate flux to the Gulf of have now been converted to other land uses and Mexico. the percentage of inland swamps and riparian wet- Landscape practices, such as maintaining buffer lands lost is even greater (Mitsch and Gosselink strips between cultivated fields and nearby streams, 2000). Many floodplains have been disconnected moderating excessive drainage by ditches and tile from their rivers by flood control projects or agri- lines, and maintaining wooded riparian areas can cultural conversion and no longer serve as nutrient further reduce the leakage of agricultural nutrients sinks. to surface waters. By combining these approaches Reducing and controlling diffuse sources of land a significant portion of the edge-of-field N losses runoff must involve large-scale landscape manage- can be reduced (Boesch and Brinsfield 2000; merit, including restoration of riparian zones and Mitsch et al. 2001). wetlands and management of lakes and reservoirs Animal wastes are a significant source of nutri- that serve as nutrient sinks. Mitsch et al. (2001) ent pollution from agriculture. Although the total estimated that restoring 5 million acres of wetlands production of livestock has not dramatically in- in the Mississippi River Basin would reduce N load- creased in recent years, the number and size of ing to the Gulf of Mexico by 90%. The Chesapeake concentrated animal feeding operations have. Vol- Bay Program is striving to reforest 3,200 km of ri- atilization of ammonia and its subsequent deposi- parian zones and restore 10,000 ha of wetlands by tion on water bodies or their watersheds is an im- 2010 in order to achieve nutrient reduction goals portant source of N loading near areas of intense (Boesch et al. 2001a). The Danish Action Plan on animal production (Paerl et al. 2002). Enclosures the Aquatic Environment calls for re-establishment or trapping devices may eventually be required to of 16,000 ha of wet meadows as nutrient sinks stem ammonia emissions from animal wastes. Ma- (Conley et al. 9002). nure management also presents a risk of pollution Nutrient sinks can also be enhanced within if holding facilities fail or do not function properly. coastal ecosystems. Tidal wetlands serve as nutrient Because of the intensification of animal produc- sinks, and facilitating the development of deltaic tion, too much manure can be produced within a wetlands could remove a portion of the rive>borne geographic area for it to be applied to nearby land nutrients discharged to coastal waters in regions without overloading soils with nutrients (NRC such as the Mississippi delta (Mitsch et al. 2001). 2000; Sharpley 2000). The Chesapeake Bay Program has a goal of a 10- Urban runoff can also be an important diffuse fold increase in oyster biomass in order to recover source of nutrients. Reduction and control of ur- the natural biofiltration capacity (Boesch et al. ban and suburban diffuse sources can be achieved 2001a). Biodeposits associated with oyster reefs ex- through reductions in fertilizer use; effective and hibit very high rates of denitrification (Newell et well-maintained stormwater collection systems (re- al. In press). Rebuilding tidal flats that have been tention ponds can remove 30-40% of the total N lost and degraded as a result of the extensive coast- and 50-60% of the total P); and improved septic al development within Japanese bays is estimated systems that promote denitrification (NRC 2000). to be an important purifying mechanism to reverse Preservation and restoration of riparian zones and eutrophication of those ecosystems (Susuki 2001) streams within urban and suburban areas is also an important aspect of effective nutrient control. The TARGETING ability of streams to function effectively in nutrient Geographically targeting source controls and n- removal is compromised when a significant por- parian and wetland restoration is critical to the ef- tion of their watersheds is covered by impervious fectiveness of these efforts in controlling nutrient surfaces and the amplified runoff scours the loadings downstream. Statistical models based on stream beds (Booth and Jackson 1997). water quality measurements throughout the Missis- sippi River Basin show that the percentage of N SINKS leached from a field that reaches the Gulf of Mex- Removing or sequestering pollutants as they are ico depends greatly on its proximity to larger transported downstream can also abate nutrient streams and rivers (Alexander et al. 2000). Biolog- pollution. Many American and European water- ical uptake and denitrification are already effective sheds were once spongeqike, containing extensive in small watercourses, particularly if they are in flood plains and wetlands that slowed the flow of healthy condition (Peterson et al. 2001). Agricul- water and served as sinks for dissolved and sus- tural source controls should be directed in partic- pended nutrients through sedimentation, long- ular to those lands that are disproportionately re- term storage in plant biomass or denitrification. sponsible for loads delivered to coastal waters. Res- Well over half of the wetlands present in the con- toration of riparian and wetland habitats along Science and Reducing Over-enrichment 897

moderate to large streams should also be more lution and flushing by freshwater inflow and tidal cost-effective. Because of equity considerations, prism volumes to yield susceptibility indicators of- however, both incentives (subsidies and cost shar- fer a good first step. ing, technical assistance, and insurance) and dis- incentives (regulatory controls, taxes, and fees) for DEFINE DESIRABLEAND ACHIEVABLE OUTGOMES abatement tend to be applied relatively uniformly. Goals or standards for ecosystem protection or rehabilitation represent compromises based on Challenges and Opportunities for Science what is desirable and what is achievable. Gloern's With the turn of the century, the science of eu- (2001) fourth question is germane to determining trophication faces very different challenges and desirable states for the ecosystem: How does coast- opportunities. The emphasis during the late 90th al eutrophication impact the Earth system as hab- century was documentation of the degradation of itat for humanity? Answering this question requires coastal ecosystems and diagnosis of its root causes. knowledge of the consequences at higher trophic With the scope, consequences, and causes of coast- levels (e.g., fisheries) of direct importance to hu- al eutrophication now largely well documented (al- marls, but also the consequences to ecosystem ser- though this is clearly less the case in the develop- vices, the global climate system, and human health ing world), science must transition to a preventa- and culture. Science should also add realism in the tive and rehabilitative stage, with an emphasis on definition of achievable outcomes and the con- prognosis and treatment. Difficult challenges as straints, costs, and choices implicitly embedded well as exciting opportunities face the scientific therein. Science needs to remind management community and environmental managers in deter- and policymaking that ecosystems are dynamic and mining susceptibility, defining outcomes that are variable and are subject to long-term changes such both achievable and desirable, reducing sources, as estuarine infilling, deltaic senescence, and cli- enhancing sinks, targeting efforts for optimum ef- mate change. The potential consequences of 21st fect, and forecasting and observing responses. century climate change on eutrophication and outcome goals (Justi~ et al. 1996; Naijar et al. 2000) DETERMINE SUSCEPTIBILITY should be brought into consideration. Outcome Improved understanding of the degree and na- goals need to take into account the variability and ture of susceptibility of coastal ecosystems to nutri- secular changes that may take place within and be- ent over-enrichment is required not only for tar- yond environmental management horizons. geting efforts to protect threatened systems (NRG 2000; Greening and Elfring 2002), but also for REDUCE SOURCES managing the rehabilitation of ecosystems degrad- Grappling with the challenges of reducing dif- ed by multiple stresses. Three of the five questions fuse nutrient sources, tracking the downstream fate posed in Gloern's (2001) review of the science of of nutrients, and understanding coastal ecosystem coastal eutrophication are directly relevant to the responses presents an exciting opportunity for the objective of determining susceptibility: How does development of holistic environmental science that the coastal ecosystem filter work? How does nutri- transcends atmospheric, terrestrial, aquatic, estua- ent enrichment interact with other stressors? How rine, and marine environments. Except for biogeo- are responses to multiple stressors linked? These chemists and engineers who develop transmedia multiple stressors include translocation of species, budgets and models, few scientists seem prepared habitat loss, fishing, inputs of toxic contaminants, to delve beyond the boundaries of their medium- manipulation of freshwater flows, aquaculture, and centric disciplines. This is unfortunate because im- climate change. portant insights can be developed and contribu- Comparative analyses of the responses of coastal tions made by those prepared to make the trip. ecosystems to nutrient enrichment are emerging, This is particularly the case for the development but have not yet developed a comprehensive un- of effective and efficient source controls, where the derstanding of these responses on a global scale agricultural scientist may develop new ideas for (Gloern 2001). Massive amounts of information source controls by understanding downstream fate are accruing from monitoring and research pro- and coastal responses or the coastal ecologist may grams that should make such a grand synthesis contribute important insights on the effectiveness possible. From a practical standpoint, this is nec- of various nutrient controls or interactions among essary to guide protection and rehabilitation ef- N, P, and silica. Science and technology to improve forts to where they are most needed and to avoid the effectiveness of nutrient source controls, both costs of controls where they have little result. Ap- from diffuse sources and in advanced waste treat- proaches described in the NRG (2000) assessment ment, must be a high priority in the preventative for classifying estuaries and bays according the di- and rehabilitative stage of eutrophication assess- 898 D.F. Boesch

merit and management. This requires not only in- critical to determining the effectiveness of abate- tensive agronomic research, for example, but also ment strategies, evaluating outcomes with respect placing this research into a broader landscape and to goals, and placing the responses into the con- watershed context. text of ecosystem variability, To be effective in an adaptive management ENHANCE SINKS framework, modeling and monitoring should be Science and ecotechnology related to enhancing intimately coupled but seldom are. Models of en- nutrient sinks must also be a high priority in the vironmental processes as complex as watershed prognosis and treatment of eutrophication. As with transport and nutrient and community dynamics source controls, they should also be conducted within coastal ecosystems can be simulated only within a landscape and seascape context. Key issues with significant uncertainty (Cloern 2001), Over- include the strategic siting of ponds, wetlands, and reliance on single, cross-scale models of biophysi- riparian buffers within the landscape and along wa- cal processes was identified by Walters (1997) as ter courses (Mitsch et al. 2001); their operation one of the principal impediments to the imple- and maintenance; and effective design of coastal mentation of adaptive management, Focusing ex- and estuarine habitat restoration to enhance coast- clusively on monitoring results without incorporat- al nutrient sinks such as salt marshes, tidal flats, ing predictive modeling has been a criticism lev- seagrass beds, and oyster reefs. eled at the Danish monitoring and assessment program (Conley et al, 2002), The pursuit of TA~CET EVVORTS outcome-based, TMDL-like strategies for reducing Geographic information systems and spatially ex- nutrient over-enrichment to desirable and achiev- plicit models enhance the ability for targeting of able levels requires avariety of modeling approach- source reduction and sink enhancement efforts. es----simple and complex, statistical and mechanis- SPARROW (Spatially Referenced Regressions on tic-integrated with monitoring observations in Watersheds) modeling based on observed water the adaptive implementation of management pro- quality data provides an empirical, strategic tool grams (NRC 2001). for this on regional scales (Smith et al. 1997). Mechanistic watershed models of process rates and ACKNOWLEDGMENTS states allow one to estimate delivered nutrient I thank Catherine Schmitt for her assistance in background loads resulting from source reductions on progres- research, Nancy N. Rabalais for her long-term commitnaent and sively finer special scales, but, of course, are sen- patience, James N. Galloway for global N fixation data included sitive to model assumptions (NRC 2000). Spatially in Fig. 2, and two anonymous reviewers for improvements to the manuscript. explicit process models can even incorporate economic drivers and costs (Costanza et al. 2002). Re- LITERATURE CITED search on source controls and sink enhancement should be more effectively linked with such mod- ~ER, R. g., R. A. SMrrH, AND G. E. SCHWARTZ.2000. Effect of stream channel size on the delivery of nitrogen to the GuK eling approaches. Management intervention, for of Mexico. 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Biological Re- PREDICT AND OBSERVE RESPONSES source Management: Connecting Science and Policy. Spling- er, Berlin, Germany. Efforts to reduce nutrient over-enrichment of BOESCH, D. F., R. BI~NSrIELD,AND R. MAGNmN. 2001a. Chesa- coastal ecosystems must place a premium on en- peake Bay eutrophication: Scientific understanding, ecosys- vironmental modeling and monitoring (NRC tem restoration, and challenges for agriculture. Journal of En- oironmental Quality 30:303-320. 2000), particularly if they involve controlling mul- BOESCH, D., E. BLrRRESON,W. DENNmON, E. HotmE, M. KEN~,V. tiple sources within a watershed (NRC 1999). Fore- ~u R. NEWELL, K. PAUXrrER,R. ORTH, AND R. ULANOW- cast models are needed not only to target abate- ICZ. 200lb. Factors in the decline of coastal ecosystems. Science ment, but also to track the consequences of source 293:1589-1590. BOOTIe, D. B. AND C. R. JACKSON. 1997. 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