- Email: [email protected]
Cultural eutrophication of shallow coastal waters: Coupling changing anthropogenic nutrient inputs to regional management approaches
LIMNOLOGICA
Limnologica 29 (1999)249-254 http://www.urbanfischer.de/j oumals/limno
© by Urban & Fischer Verlag
Institute of Marine Sciences, University of North Carolina at Chapel Hill, North Carolina, U.S.A.
Cultural Eutrophication of Shallow Coastal Waters: Coupling Changing Anthropogenic Nutrient Inputs to Regional Management Approaches HANS W. PAERL With 2 Figures and 2 Tables Key words: Primary production, nutrients, eutrophication, atmospheric deposition
Abstract Coastal waters comprise only about 15% of the world's ocean area, yet account for nearly half of its primary and secondary production (WOLLAST1991). This disparity can in part be traced to anthropogenic nutrient, specifically nitrogen (N), loading. Regionally, Nsensitive coastal waters are experiencing unprecedented nutrientdriven eutophication, deteriorating Water quality (i.e. hypoxia, anoxia, toxicity), habitat loss and declines in desirable fish stocks and yields. In most coastal regions externally-supplied "new" nutrient inputs are growing, diversifying and changing as a result of urbanization, industrial and agricultural development. In some cases (e.g. Eastern Europe), declining economic condition shave led to a reversal of this scenario. A need exists to identify key nutrient sources (and changes therein) supporting eutrophication and its socio-economic consequences. While we are addressing and managing terrestrial (i.e. point and non-point source runoff) "new" nutrient inputs, key "out of sight out of mind" anthropogenic nutrient sources and their effects on eutrophication remain poorly understood and managed. These include atmospheric deposition and groundwater, which can account for as much as half the "new" N entering North American (U.S. Atlantic East Coast) and European (Baltic Sea) coastal waters. Here, I will examine these emerging nutrient sources and their roles in shallow coastal biogeochemical and trophodynamics alterations. Technological and conceptual tools and approaches aimed at improving our functional understanding of these and other "new" nutrient-eutrophication interactions are discussed.
Introduction Shallow coastal waters are under the ever-increasing influence of anthropogenic nutrient loading. Among externallysupplied or "new" nutrients, nitrogen (N) is the "currency" controlling primary production and eutrophication in North American and European (Baltic, North Sea, Mediterranean) N-sensitive shallow estuarine and coastal waters (termed
coastal waters) (RYTHER & DUNSTAN 1971; D'ELIA et al. 1986; GRANt~LIet al. 1990; NIXON 1995). Because new N sources are growing, diversifying and changing, identifying and characterizing sources, their transport, biogeochemical and ecological fates are of prime concern in assessing and managing impacts of cultural eutrophication (hypoxia/anoxia, toxicity, food chain alterations, fisheries declines). The most rapidly-growing (both in terms of input and geographic scale) sources of anthropogenic N loading are atmospheric deposition (AD) and groundwater (GW). Approximately 20 to 40% of new N input into coastal waters is of atmospheric origin, virtually all of it attributable to growing agricultural, urban and industrial emissions (Table 1). AD alone contributes from 200 to over 1000 mg N • m -2 • y 1 in coastal waters (DvcE et al. 1991; PAERL 1993, 1995). The relative contribution of AD-N to coastal N budgets will increase substantially as we enter the next century, when nearly 70% of the US and more than 60% of the European human populations will reside within 75 km of the coast. In North America, volatilization of ammonia from rapidly-expanding livestock and poultry operations in upwind watersheds represents an additional, growing source of"new" N in coastal waters. Globally, AD-N is a highly significant contributor to oceanic new N inputs, accounting for =35 TgN. y-l, compared to 30 TgN. y-1 from runoff and riverine discharge, 5-10 TgN • y-1 for groundwater and --8 TgN- y-1 for biological nitrogen fixation (CoDtsPOTI et al. 1999). In many regions, AD-N is the single most important source of new N currently impacting the coastal zone. As such, it is imperative that we assess the biogeochemical and trophic ramifications of this previously "out of sight out of mind" source of new N. Increasing rates of new N deposition from this recently-recognized source may be linked to accelerating eutrophication and an "epidemic" of harmful (toxic, hy0075-9511/99/29/03-249 $ 12.00/0
249
Table 1. Estimated contributions of atmospherically-derived N (ADN) to the total "new" N inputs in diverse coastal waters. Data are based on either direct wet (D) deposition (i.e. dry deposition is not included), or direct plus watershed-based indirect deposition (DI). Data from PAERL(1993). Receiving Waters
% of "new" N as ADN
Deposition Type
Baltic Sea (Proper) >25% Baltic Sea Region =40% Baltic Sea (Kiel Bight) 60% Baltic Sea (Danish Coastal Waters) =35 %
D DI D D
North Sea (Coastal)
DI
=25 %
Western Mediterranean Sea Narragansett Bay, U.S.A.
namically (NIXON 1995; RIEGMAN 1990; SMETACEKet al. 1991). Biogeochemical impacts are defined as affecting material fluxes (e.g. C, N, organic matter). Trophodynamic impacts include alterations of primary producer and higher consumer level community composition (i.e. biodiversity), food web structure and function. The two types of impacts overlap in the context of ecosystem-level responses to nutrient perturbation. For example, nutrient-enhanced primary production leads to elevated rates of CO2 fixation, production and accumulation of phytoplankton, benthic microalgal and macrophyte biomass. Accompanying this are increased rates of respiration and decomposition, which in turn affect [02] and [CO2], nutrient chemical forms and cycling characteristics. Typically, biodiversity is reduced as specific taxa able to most effectively exploit nutrient enrichment (i.e. "gulpers") and associated environmental changes (e.g. hypoxia, anoxia) outcompete less opportunistic species. Nutrient-enhanced acceleration of plant production,, accompanied by a community change to rapidly-proliferating taxa is commonly referred to as eutrophication. Eutrophication embodies numerous biogeochemical and trophic "feedback" loops (Fig. 1), each of potential consequence to water quality, trophic and resource value of affected impacted waters. From a nutrient management perspective, both biogeochemical and trophic ramifications of eutrophication must be considered and weighed with respect to decision making based on the value of the resource (economically and ecologically) and the cost of protecting and managing it. Coastal ecosystems undergoing eutrophication exhibit large spatial and temporal oscillations in production and consumption of organic matter, pO2 and pCO2, all of which are of consequence to water and habitat quality (Fig. 1).
10-60%
DI
5-20%
DI
New York Bight, U.S.A.
=40%
DI
Chesapeake Bay, U.S.A.
=35%
DI
Neuse River-Pamlico Sound, N.C., U.S.A.
28-38 %
DI
Atlantic Ocean Coastal Waters, N.C., U.S.A.
35-60%
DI
poxia/anoxia generating) algal blooms invading coastal waters and beyond (PEARL1988; HALLEGRAEFF1993).
Biogeochemical, trophic, water quality and resource impacts of nutrient enrichment in coastal waters: current perspectives Nutrient enrichment impacts coastal resources in 2 distinct, but interrelated ways: biogeochemically and throphody-
Atmospheric Deposition
Runoff
/~
L_J
PrimsryProduction ~
Secondary+Tertiary
.~
Ox~en Dynamics ~
...............+++++..++++++++++ NutrientLoading(increasing)
../// r
........... _.+++-- . . / I
llme
250
Limnologica 29 (1999) 3
/
/ Fig. 1. Impacts of anthropogenically-enhanced nutrient loading on coastal biogeochemistry, trophodynamics and water quality. Note the numerous potentially negative feedbacks which come into play in response to increased eutrophication (i.e. accelerating primary production).
Fig. 2. Schematic diagram of physical, chemical and biotic interactions in shallow coastal ecosystems determining their trophic states and water quality. (Adapted from PAEaL1997.)
Optimally, we should manage for maximum production, while avoiding excessive 02 "sags" or depletion events, resulting in a loss of biodiversity and habitat, and the appearance and persistence of harmful (i.e. toxic, hypoxia/anoxia promoting) algal bloom species. To do this, we must understand physical (meteorological, hydrologial, morphological, optical) constraints or "forcing" on the ecosystem in question (Fig. 2). Estuarine and coastal "sensitivity" to the detrimental effects of eutrophication depends on physical features such as morphometry, water retention and flushing rates, mixing depths and rates, transparency, temperature, salinity and resultant density gradients. The extent to which an ecosystem can assimilate and process nutrients and organic matter (i.e. assimilative capacity) and exhibit varying degrees of eutrophication is dependent on integrating physical features with chemical and biological effectors (Fig. 2). Nutrient-driven eutrophication is not a "one way" proposition. Biogeochemical and trophic alterations can, in turn, modify the habitat physically (e.g. altered light penetration), chemically (sediment and water column nutrient release and bioavailability), and biologically (hypoxia and anoxia related to habitat alteration, grazing, mutualistic and symbiotic interactions). These feedbacks can have large "internal" impacts on nutrient cycling, growth and production. Ecosystem-level physical-chemical-biological modeling will prove valuable in parameterizing and predicting eutrophication potentials based on externally-supplied "new" and internally regenerated nutrient input and cycling dynamics. This is a critical ingredient for meaningful and effective management of coastal water production, nutrient and biomass assimilative capacity and resultant water quality.
Identifying sources, routes and fates of "new" nutrients in coastal waters We need to identify sources, routes and fates of AD-N as they impact coastal water quality, biotic and economic sustainability. It is clear that AD and GW sources and fates do not stop at international boundaries; therefore, assessment tools and management approaches must minimally be regional in scale.
Atmospheric deposition of nitrogen Regional anthropogenic activities responsible for AD-N include: fossil fuel combustion and biomass burning (NO2-1/ NO3-1, NH3/NH4+), agricultural waste and fertilizer volatilization (NH3), and unknown sources of dissolved organic nitrogen (DON) (BuIJSMAN et al. 1987; TIMPERLEYet al. 1987; DUCEet al. 1991; CORNELLet al. 1995). GW-N sources include seepage of urban and agricultural wasters and fertilizers (NO3-, NH4-, DON). Changing (largely increasing) amounts of these biologically "reactive" forms of N reflect altered demography, industrial and agricultural activities (RODHE & ROOD 1986; GALLOWAYet al. 1994). We are concerned about both amounts and composition of AD-N and GW-N inputs, since they profoundly impact algal production and community composition (e.g. harmful vs. non-harmful algal blooms). A chief source of atmospheric-N emitted from agricultural (animal operations) waste is ammonia (BuIJSMAN et al. 1987). In Western European and North American animal operations involving wastewater lagoons or terrestrially-applied wastes, it is estimated that approximately 25 to over 70% of the nitrogen discharged may be "lost" as volatilized Limnologica 29 (1999) 3
251
NH3 (SOMMER et al. 1993). In Western Europe, NH 3
volatilization is now recognized as one of the most important sources of N enrichment threatening surface water quality in N-sensitive estuarine and coastal waters (ASMANet al. 1994). PAERLet al. (1995) showed that coastal rainfall collected at Morehead City, N.C., U.S.A. (UNC-IMS) can, at times, exhibit very high concentrations of ammonium (>75 ~M). High ammonium rainfall appears to be associated with local weather and storm fronts from agricultural regions to the west, while storms of oceanic origin (east) contain only traces of ammonium. We suspect that agricultural emissions may, in part, be responsible for elevated ammonium levels in rainfall. Fossil fuel combustion and biomass burning release large quantities of nitrogen oxides (NOx), which in many regions comprise the single largest component of AD-N (DucE et al. 1991; PAERL1995). Dominant sources of NOx include; automobiles, electric power plants, forest, range and cropland burning (GALLOWAYet al. 1994). As a nutrient, NOx (NO2-~ + NO3-1) is readily assimilated by phytoplankton and attached plants. This AD-N source has increased most rapidly in developing countries. The dynamics of the generation, transport and fate of these relatively large atmospheric N sources require assessment in the context of managing large scale biogeochemical and trophic impacts. This appears to be a task well-suited for stable isotope analysis. Fortuitously, the isotopic "signature" (5 15N) of dominant N species implicated in atmospheric emission of animal wastes (NH3/NH4 +) and fossil fuel combustion (NOx) are quite distinct (in the case of NH4+ very negative, on the order o f - 7 to -12) from other anthropogenically-generated N sources (i.e. fertilizers, sewage) currently being discharged in surface and groundwater (HEATON 1986). The unique "signature" of atmospherically-derived ammonia/ammonium can serve as a "tracer" of the generation, transport and fate of this important N source (PAERL& FOGEL 1994) (Table 2). In combination with rainfall and
Table 2. Stable nitrogen isotope (5 15N)values (ranges shown) for dominant externally-supplied (new) and internally-supplied (i.e. regenerated) N sources in coastal waters. N Source
~ 15N
N2 in air Remineralized NH4 (estuarine) Sewage Effluent: NH4+ NO3-
0.0 +10.0 to + 16.0 +5.0 to + 11.0 +5.0 to +10.0
Agricultural Land Runoff Fertilizers (Synthetic) Atmospheric Deposition: NH4+ NO3-
+8.0 to + 10.0 -2.0 to +2.0 -13.0 to +2.0 -5.0 to +2.0
References: VELINSKIet al. (1989); FOGEL& CIFUENTES(1993); PAERLet al. (1993). 252
Limnologica 29 (1999) 3
runoff ammonium concentration and loading determinations, we now have the technical capabilities for assessing the butgetary and environmental impacts of these N sources on the ecosystem level.
Groundwater The advent of "modem" agricultural practices, urbanization and industrialization have brought unprecendented use and contamination of groundwater. In coastal regions, relatively shallow aquifers, combined with concentrated human activities, haveput intense pressure on this resource. The use of groundwater for drinking, industrial and agricultural (i.e. irrigation) purposes, combined with ever-increasing applications of synthetic and organic fertilizers, wastes and xenoNotic compounds has led to rapid nutrient enrichment of groundwater. This is especially true for nitrogen, a key component of fertilizers and wastes, whose chemical forms are largely mobile and biologically-reactive. While our understanding of the biogeochemistry of N and other nutrients in groundwater is rudimentary, coastal aquifers residing near anthropogenic N sources reveal varying levels of N contamination, ranging from mM to M concentrations (CAPONE & BAUTISTA 1985; CHURCH 1996). Groundwater N input (into coastal waters) budgets are not well-established; however, this "new" N source can be quantitatively significant (JoHANNES 1980; CAPONE& BAUTISTA1985). Groundwater inputs into the coastal South Atlantic Bight (Georgia-South Carolina) may be equivalent to riverine discharge (MOORE 1996). Clearly, groundwater inputs should be factored into shallow coastal nutrient (especially N) budgets. The relative importance of GW as a source of "new" N is growing. This is particularly true in the coastal agricultural regions of the mid-Atlantic supporting expanding irrigated row-crop, silviculture, livestock and poultry operations. With respect to the latter, coastal North Carolina offers a prime example of groundwater N enrichment from a rapidlyexpanding animal industry. Within half a decade, a significant portion (N25%) of North Carolina's Coastal Plain has been converted from forest and row-crops (corn, soybeans, tobacco) to animal (mostly swine and poultry) operations; a growing percentage of this region's surface area is now covered with animal wastewater lagoons and adjacent fields on which wastes are directly applied as a source of fertilizer. While approximately 1 million production hogs existed in 1990, the current count is approximately 10 million; most are concentrated near the coast. Hogs now outnumber humans by a factor of 2.5. This "explosion" of animals has created a huge waste problem which to date remains largely unresolved. Wastewater lagoons and land-applied waste have been shown to lose substantial amounts of N to groundwater. While land-based animal waste applications are a relatively new phenomenon in the U.S. Atlantic coastal region, this practice has long been in place in Europe's coastal regions (Benelux, France, U.K., Germany, Denmark, Poland).
Recognition of the problem has led to improved management in some regions, with marked reductions in groundwater N contamination. In regions experiencing agricultural economic downtums (Eastern Europe), groundwater N contamination has decreased. Groundwater N contamination continues to be an unabated and growing problem in the U.S. and other agriculturally and industrially "developing" countries. Nitrogen is not be the only accelerating "new" nutrient source to which estuarine and coastal waters exhibit sensitivity. Iron, a variety of trace metals and to a lesser extent phosphorus are also deposited via anthropogenically-enhanced atmospheric and groundwater inputs (CHURCHet al. 1984). Iron additions to some pelagic and coastal oceanic waters are capable of stimulating primary production. Fe and N may interact in a synergistic manner in these waters to enhance primary production (MARTIN et al. 1994; TAKEDAet al. 1995; PAERLet al. 1999) and alter phytoplankton community composition (D~'TuLuo et al. 1993). Fossil fuel combustion, industrial and agricultural emissions, and desertification (as a result of changing land use and vegetation removal) all enhance atmospheric and groundwater Fe and other trace metal emissions and discharges. These hitherto-neglected, but potentially-important, means of stimulating coastal primary production require examination and evaluation. The functional and geographic linkage to accelerating eutrophication and the increased frequency of diverse of phytoplankton blooms should be investigated. Research and management questions addressing this issue include: 1) What are the stoichiometric and functional relationships between externally-supplied "new" nutrient inputs and eutrophication? 2) Is there a functional link between increased "new" nutrient inputs and harmful phytoplankton bloom taxa? 3) Are there unique properties of "new" nutrient sources (N, Fe, trace metals) and combinations thereof, that make them effective agents for supporting harmful blooms and associated water quality degradation (hypoxia, anoxia, toxicity)? 4) What sequences of nutrient loading events are necessary for accelerating eutrophication, initiating and sustaining algal blooms? How do acute and chronic "new" and regenerated loading events translate into enhanced phytoplankton community alterations and bloom formation? 5) What are the relevant spatial (cm, m, kin, 100's of kin, etc.) and temporal (rain, h, d, yr, decades, etc.) scales of nutrient-production interactions we must consider for appropriately assessing, modeling and managing eutrophication dynamics in shallow coastal environments? 6) What roles do synergistic interactions of physical, chemical (nutrient) and biotic (grazing, nutrient regeneration, consortial interactions) factors play in coastal eutrophication dynamics? 7) What microbiological, molecular, analytical and geochemical tools are available and suitable for addressing the above-mentioned research and management questions?
8) How can we best use and integrate existing and evolving remote sensing (aircraft, satellite) technologies to link process research to large scale, synoptic nutrient-production interactions?
What is needed from a coastal research and management perspective? Because ADN and GW represent large and growing sources of "new" N, the dynamics of their formation, transport, deposition and utilization must be clarified and incorporated in management strategies aimed at controlling and reversing cultural eutrophication. Relevant methods, research and management approaches are outlined below. 1) Tools and technologies capable of identifying and tracing local and regional N sources as they impact coastal water quality. Dominant new N inputs exhibit unique stable N isotope (5 15N) "signatures", which may be utilized as tracers. 2) A functional understanding of how new N (and other nutrient) inputs translate into coastal production and food web alterations. Diagnostic plant pigment, physiological and molecular (immunochemical and nucleic acid-based) identification and characterization tools are increasingly-available for this purpose. 3) Complementing technologies with appropriate (i.e. scale and sensitivity) remote sensing and land use characterization (GIS) approaches so that we can we link specific N inputs to coastal biogeochemical and trophic changes. Applications of these technologies will also facilitate regional comparisons of nutrient-production interactions. 4) Determine to what extent nutrient impacts on coastal production are local, regional or global phenomena. 5) Determine the economic and social costs and tradeoffs of water quality management strategies based on the above approaches and resultant criteria.
Acknowledgements: Research support was provided by the National Science Foundation, Projects OCE 9115706, DEB 9210495 and DEB 9220886. Additional support came from the National Sea Grant Office (NOAA), in conjunction with the North Carolina Sea Grant College Program (Projects R/EHP-1, R/MER-23 and R/MER30), and the U.S. Geological Survey/UNC Water Resources Research Institute (Project UNC-790-2). The U.S. Environmental Protection Agency (Air Quality Laboratory, Research Triangle Park, NC) provided atmospheric N deposition data through the regional atmospheric deposition model (RADM).
References ASMAN, W. A. H., HARRISON, R. M. & OTTLEY, C. J. (1994): Estimation of net air-sea flux of ammonia over the southern bight of the North Sea. Atmosph. Environ. 28: 3647-3652.
Limnologica 29 (1999) 3
253
BRIBLECOMBE,P. & STEDMAN,D. H. (1982): Historical evidence for a dramatic increase in the nitrate component of acid rain. Nature 298: 460-462. BUIJSMAN,E., MAAS, H. E M. & ASMAN,W. A. H. (1967): Anthropogenic amonia emissions in Europe. Atmosph. Environ. 21: 1009-1020. CAPONE, D. G. & BAUTISTA,M. E (1985): A groundwater source of nitrate in nearshore marine sediments. Nature 313: 214-216. CHURCH, T. M. (1996): An underground route for the water cycle. Nature 380: 579-580. -- TRAMONTANO,J. M., SCUDLARK,J. e., JICKELLS,T. D., TOKOS,J. J. & KNAPP,A. M. (1984): The wet deposition of trace metals to the western Atlantic Ocean at the mid-Atlantic coast and on Bermuda. Atmosph. Environ. 18: 2657-2664. CODISPOTI, L. A., CHRISTENSEN,J., DEVOL, A., PAERL, H. W. & YOSHINARI, T. (1999): The influence of an unbalanced oceanic combined nitrogen budget on atmospheric carbon dioxide. Mar. Chem. (in press). CORNELL, S., RENDELL,A. & JICKELLS,T. (1995): Atmospheric inputs of dissolved organic nitrogen to the oceans. Nature 376: 243-246. D'ELIA, C. R, SANDERS,J. G. & BOYNTON,W. R. (1986): Nutrient enrichment studies in a coastal plain estuary: phytoplankton growth in large scale, continuous cultures. Can. J. Fish. Aquat. Sci. 43: 397-406. DPTuLLIO, G. R., HUTCHINS,D. A. & BRULAND,K. W. (1993): Interaction of iron and major nutrients controls phytoplankton growth and species composition in the tropical North Pacific Ocean. Limnol. Oceanogr. 38: 495-508. DUCE, R. A. et al. (1991): The atmospheric input of trace species to the world ocean. Global Biogeochem. Cycles 5: 193-259. GALLOWAY,J. N., LEVY II, H. & KASIBAHTLY,P. S. (1994): Year 2020: Consequences of population growth and development on deposition of oxidized nitrogen. Ambio 23: 120-123. GRANELI, E., WALLSTROM,K., LARSSON,U., GRANI~LI,W. & ELMGREN, R. (1990): Nutrient limitation of primary production in the Baltic Sea area. Ambio 19: 142-151. HALLEGRAEEE,G. (1993): A review of harmful algal blooms and their apparent global increase. Phycologia 32: 79-99. HEATON,T. H. E. (1986): Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere. Chem. Geol. 59: 87-102. MARTIN, J. H. et ai. (1994): Testing the iron hypothesis in ecosystems of the equatorial pacific ocean. Nature 371: 123-129. MATSON,E. A. (1993): Nutrient flux through soils and aquifers to the coastal zone of Guam (Mariana Islands). Limnol. Oceanogr. 38: 361-371. MOORE,W. S. (1996): Large groundwater inputs to coastal waters revealed by 226Raenrichments. Nature 380:612-614. NIXON, S. W. (1986): Nutrient dynamics and the productivity of marine coastal waters. In: HALWAGY,R., CLAYTON,D. & BEHBEHANI, M. (eds.), Coastal Eutrophication, pp. 97-115. Oxford. - (1995): Coastal eutrophication: A definition, social causes, and future concerns. Ophelia: 199-220. PAERL,H. W. (1985): Enhancement of marine primary production by nitrogen-enriched acid rain. Nature 315: 747-749.
254
Limnologica 29 (1999) 3
(1988): Nuisance phytoplankton blooms in coastal, estuarine and inland waters. Limnol. Oceanogr. 33: 823-847. - (1993): Emerging role of atmospheric nitrogen deposition in coastal eutrophication: Biogeochemical and trophic perspectives. Can. J. Fish. Aquat. Sci. 50: 2254-2269. - (1997): Coastal eutrophication and harmful algal blooms: importance of atmospheric deposition and groundwater as "new" nitrogen and other nutrient sources. Limnol. Oceanogr. 42:1154-1165. - & FOGEL, M. L. (1994): Isotopic characterization of atmospheric nitrogen inputs as sources of enhanced primary production in coastal Atlantic Ocean waters. Mar. Biol. 119: 635-645. - RUDEK,J. & MALLIN,M. A. (1990): Stimulation of phytoplankton production in coastal waters by natural rainfall inputs: nutritional and trophic implications. Mar. Biol. 107: 247-254. -- MALLIN, M. A., DONMAHUE, C. A., Go, M. & PEIERLS, B. L. (1995): Nitrogen loading sources and eutrophication of the Reuse River estuary, NC: Direct and indirect roles of atmospheric deposition. Report No. 291. Univ. of N. Carolina Water Resources Research Instit., Raleigh, NC, 119 p. - WILLEY, J. D., GO, M., PEIERLS, B. L. & FOGEL, M. L. (1999): Rainfull stimulation of primary production in western Atlantic Ocean waters: roles of different nitrogen sources and co-limiting nutrients. Mar. Ecol. Progr. Ser. 176: 205-214. RIEGMAN, R. (1990): Mechanisms behind eutrophication-induced novel algal blooms. N.I.O.Z. Rapport 9: 1-51. RODHE, H. & ROOD, J. M. (1986): Temporal evolution of nitrogen compounds in Swedish precipitation since 1955. Nature 321: 762-764. RYTHER,J. H. & DUNSTAN,W. M. (1971): Nitrogen, phosphorus and eutrophication in the coastal marine environment. Science 171: 1008-1112. SMETACEK, V., BATHMANN, U., N(~THIG, E.-M. & SCHAREK, R. (1991): Coastal Eutrophication: Causes and consequences. In: MANTOURA,R. C. E, MARTIN,J.-M. & WOLLAST,R. (eds.), Ocean Margin Processes in Global Change, pp. 251-279. Chichester. SOMMER, S. G., CHRISTENSEN,B. T., NIELSEN,N. E. & SCHJORRING, J. K. (1993): Ammonia volatilization during storage of cattle and pig slurry: effect of surface cover. J. Agr. Sci. 121:63-71. TAKEDA,S., KAMATANI,A. & KAWANOBE,K. (1995): Effects of nitrogen and iron enrichments on phytoplankton communities in the northwestern Indian Ocean. Mar. Chem.: 229-241. TIMPERLEY,M. H., VIGOR-BROWN,R. J., KAWASHIMA,M. & ISHIGAMI, D. M. (1985): Organic nitrogen compounds in atmospheric precipitation: their chemistry and availability to phytoplankton. Can. J. Fish. Aquat. Sci. 42: 1171-1177. WOLLAST, R. (1991): The coastal organic carbon cycle: fluxes, sources, and sinks. In: MANTOURA,R. C. E MARTIN, J.-M. & WOLLAST, R. (eds.), Ocean Margin Processes in Global Change, pp. 365-382. Chichester. -
Author's address: HANS W. PAERL, Institute of Marine Sciences, University of North Carolina at Chapel Hill, 3431 Arendell Street, Morehead City, North Carolina, 28557 U.S.A.; Fax: +252/726/2426; e-mail: hpaerl@ email.unc.edu.
Limnologica 29 (1999)249-254 http://www.urbanfischer.de/j oumals/limno
© by Urban & Fischer Verlag
Institute of Marine Sciences, University of North Carolina at Chapel Hill, North Carolina, U.S.A.
Cultural Eutrophication of Shallow Coastal Waters: Coupling Changing Anthropogenic Nutrient Inputs to Regional Management Approaches HANS W. PAERL With 2 Figures and 2 Tables Key words: Primary production, nutrients, eutrophication, atmospheric deposition
Abstract Coastal waters comprise only about 15% of the world's ocean area, yet account for nearly half of its primary and secondary production (WOLLAST1991). This disparity can in part be traced to anthropogenic nutrient, specifically nitrogen (N), loading. Regionally, Nsensitive coastal waters are experiencing unprecedented nutrientdriven eutophication, deteriorating Water quality (i.e. hypoxia, anoxia, toxicity), habitat loss and declines in desirable fish stocks and yields. In most coastal regions externally-supplied "new" nutrient inputs are growing, diversifying and changing as a result of urbanization, industrial and agricultural development. In some cases (e.g. Eastern Europe), declining economic condition shave led to a reversal of this scenario. A need exists to identify key nutrient sources (and changes therein) supporting eutrophication and its socio-economic consequences. While we are addressing and managing terrestrial (i.e. point and non-point source runoff) "new" nutrient inputs, key "out of sight out of mind" anthropogenic nutrient sources and their effects on eutrophication remain poorly understood and managed. These include atmospheric deposition and groundwater, which can account for as much as half the "new" N entering North American (U.S. Atlantic East Coast) and European (Baltic Sea) coastal waters. Here, I will examine these emerging nutrient sources and their roles in shallow coastal biogeochemical and trophodynamics alterations. Technological and conceptual tools and approaches aimed at improving our functional understanding of these and other "new" nutrient-eutrophication interactions are discussed.
Introduction Shallow coastal waters are under the ever-increasing influence of anthropogenic nutrient loading. Among externallysupplied or "new" nutrients, nitrogen (N) is the "currency" controlling primary production and eutrophication in North American and European (Baltic, North Sea, Mediterranean) N-sensitive shallow estuarine and coastal waters (termed
coastal waters) (RYTHER & DUNSTAN 1971; D'ELIA et al. 1986; GRANt~LIet al. 1990; NIXON 1995). Because new N sources are growing, diversifying and changing, identifying and characterizing sources, their transport, biogeochemical and ecological fates are of prime concern in assessing and managing impacts of cultural eutrophication (hypoxia/anoxia, toxicity, food chain alterations, fisheries declines). The most rapidly-growing (both in terms of input and geographic scale) sources of anthropogenic N loading are atmospheric deposition (AD) and groundwater (GW). Approximately 20 to 40% of new N input into coastal waters is of atmospheric origin, virtually all of it attributable to growing agricultural, urban and industrial emissions (Table 1). AD alone contributes from 200 to over 1000 mg N • m -2 • y 1 in coastal waters (DvcE et al. 1991; PAERL 1993, 1995). The relative contribution of AD-N to coastal N budgets will increase substantially as we enter the next century, when nearly 70% of the US and more than 60% of the European human populations will reside within 75 km of the coast. In North America, volatilization of ammonia from rapidly-expanding livestock and poultry operations in upwind watersheds represents an additional, growing source of"new" N in coastal waters. Globally, AD-N is a highly significant contributor to oceanic new N inputs, accounting for =35 TgN. y-l, compared to 30 TgN. y-1 from runoff and riverine discharge, 5-10 TgN • y-1 for groundwater and --8 TgN- y-1 for biological nitrogen fixation (CoDtsPOTI et al. 1999). In many regions, AD-N is the single most important source of new N currently impacting the coastal zone. As such, it is imperative that we assess the biogeochemical and trophic ramifications of this previously "out of sight out of mind" source of new N. Increasing rates of new N deposition from this recently-recognized source may be linked to accelerating eutrophication and an "epidemic" of harmful (toxic, hy0075-9511/99/29/03-249 $ 12.00/0
249
Table 1. Estimated contributions of atmospherically-derived N (ADN) to the total "new" N inputs in diverse coastal waters. Data are based on either direct wet (D) deposition (i.e. dry deposition is not included), or direct plus watershed-based indirect deposition (DI). Data from PAERL(1993). Receiving Waters
% of "new" N as ADN
Deposition Type
Baltic Sea (Proper) >25% Baltic Sea Region =40% Baltic Sea (Kiel Bight) 60% Baltic Sea (Danish Coastal Waters) =35 %
D DI D D
North Sea (Coastal)
DI
=25 %
Western Mediterranean Sea Narragansett Bay, U.S.A.
namically (NIXON 1995; RIEGMAN 1990; SMETACEKet al. 1991). Biogeochemical impacts are defined as affecting material fluxes (e.g. C, N, organic matter). Trophodynamic impacts include alterations of primary producer and higher consumer level community composition (i.e. biodiversity), food web structure and function. The two types of impacts overlap in the context of ecosystem-level responses to nutrient perturbation. For example, nutrient-enhanced primary production leads to elevated rates of CO2 fixation, production and accumulation of phytoplankton, benthic microalgal and macrophyte biomass. Accompanying this are increased rates of respiration and decomposition, which in turn affect [02] and [CO2], nutrient chemical forms and cycling characteristics. Typically, biodiversity is reduced as specific taxa able to most effectively exploit nutrient enrichment (i.e. "gulpers") and associated environmental changes (e.g. hypoxia, anoxia) outcompete less opportunistic species. Nutrient-enhanced acceleration of plant production,, accompanied by a community change to rapidly-proliferating taxa is commonly referred to as eutrophication. Eutrophication embodies numerous biogeochemical and trophic "feedback" loops (Fig. 1), each of potential consequence to water quality, trophic and resource value of affected impacted waters. From a nutrient management perspective, both biogeochemical and trophic ramifications of eutrophication must be considered and weighed with respect to decision making based on the value of the resource (economically and ecologically) and the cost of protecting and managing it. Coastal ecosystems undergoing eutrophication exhibit large spatial and temporal oscillations in production and consumption of organic matter, pO2 and pCO2, all of which are of consequence to water and habitat quality (Fig. 1).
10-60%
DI
5-20%
DI
New York Bight, U.S.A.
=40%
DI
Chesapeake Bay, U.S.A.
=35%
DI
Neuse River-Pamlico Sound, N.C., U.S.A.
28-38 %
DI
Atlantic Ocean Coastal Waters, N.C., U.S.A.
35-60%
DI
poxia/anoxia generating) algal blooms invading coastal waters and beyond (PEARL1988; HALLEGRAEFF1993).
Biogeochemical, trophic, water quality and resource impacts of nutrient enrichment in coastal waters: current perspectives Nutrient enrichment impacts coastal resources in 2 distinct, but interrelated ways: biogeochemically and throphody-
Atmospheric Deposition
Runoff
/~
L_J
PrimsryProduction ~
Secondary+Tertiary
.~
Ox~en Dynamics ~
...............+++++..++++++++++ NutrientLoading(increasing)
../// r
........... _.+++-- . . / I
llme
250
Limnologica 29 (1999) 3
/
/ Fig. 1. Impacts of anthropogenically-enhanced nutrient loading on coastal biogeochemistry, trophodynamics and water quality. Note the numerous potentially negative feedbacks which come into play in response to increased eutrophication (i.e. accelerating primary production).
Fig. 2. Schematic diagram of physical, chemical and biotic interactions in shallow coastal ecosystems determining their trophic states and water quality. (Adapted from PAEaL1997.)
Optimally, we should manage for maximum production, while avoiding excessive 02 "sags" or depletion events, resulting in a loss of biodiversity and habitat, and the appearance and persistence of harmful (i.e. toxic, hypoxia/anoxia promoting) algal bloom species. To do this, we must understand physical (meteorological, hydrologial, morphological, optical) constraints or "forcing" on the ecosystem in question (Fig. 2). Estuarine and coastal "sensitivity" to the detrimental effects of eutrophication depends on physical features such as morphometry, water retention and flushing rates, mixing depths and rates, transparency, temperature, salinity and resultant density gradients. The extent to which an ecosystem can assimilate and process nutrients and organic matter (i.e. assimilative capacity) and exhibit varying degrees of eutrophication is dependent on integrating physical features with chemical and biological effectors (Fig. 2). Nutrient-driven eutrophication is not a "one way" proposition. Biogeochemical and trophic alterations can, in turn, modify the habitat physically (e.g. altered light penetration), chemically (sediment and water column nutrient release and bioavailability), and biologically (hypoxia and anoxia related to habitat alteration, grazing, mutualistic and symbiotic interactions). These feedbacks can have large "internal" impacts on nutrient cycling, growth and production. Ecosystem-level physical-chemical-biological modeling will prove valuable in parameterizing and predicting eutrophication potentials based on externally-supplied "new" and internally regenerated nutrient input and cycling dynamics. This is a critical ingredient for meaningful and effective management of coastal water production, nutrient and biomass assimilative capacity and resultant water quality.
Identifying sources, routes and fates of "new" nutrients in coastal waters We need to identify sources, routes and fates of AD-N as they impact coastal water quality, biotic and economic sustainability. It is clear that AD and GW sources and fates do not stop at international boundaries; therefore, assessment tools and management approaches must minimally be regional in scale.
Atmospheric deposition of nitrogen Regional anthropogenic activities responsible for AD-N include: fossil fuel combustion and biomass burning (NO2-1/ NO3-1, NH3/NH4+), agricultural waste and fertilizer volatilization (NH3), and unknown sources of dissolved organic nitrogen (DON) (BuIJSMAN et al. 1987; TIMPERLEYet al. 1987; DUCEet al. 1991; CORNELLet al. 1995). GW-N sources include seepage of urban and agricultural wasters and fertilizers (NO3-, NH4-, DON). Changing (largely increasing) amounts of these biologically "reactive" forms of N reflect altered demography, industrial and agricultural activities (RODHE & ROOD 1986; GALLOWAYet al. 1994). We are concerned about both amounts and composition of AD-N and GW-N inputs, since they profoundly impact algal production and community composition (e.g. harmful vs. non-harmful algal blooms). A chief source of atmospheric-N emitted from agricultural (animal operations) waste is ammonia (BuIJSMAN et al. 1987). In Western European and North American animal operations involving wastewater lagoons or terrestrially-applied wastes, it is estimated that approximately 25 to over 70% of the nitrogen discharged may be "lost" as volatilized Limnologica 29 (1999) 3
251
NH3 (SOMMER et al. 1993). In Western Europe, NH 3
volatilization is now recognized as one of the most important sources of N enrichment threatening surface water quality in N-sensitive estuarine and coastal waters (ASMANet al. 1994). PAERLet al. (1995) showed that coastal rainfall collected at Morehead City, N.C., U.S.A. (UNC-IMS) can, at times, exhibit very high concentrations of ammonium (>75 ~M). High ammonium rainfall appears to be associated with local weather and storm fronts from agricultural regions to the west, while storms of oceanic origin (east) contain only traces of ammonium. We suspect that agricultural emissions may, in part, be responsible for elevated ammonium levels in rainfall. Fossil fuel combustion and biomass burning release large quantities of nitrogen oxides (NOx), which in many regions comprise the single largest component of AD-N (DucE et al. 1991; PAERL1995). Dominant sources of NOx include; automobiles, electric power plants, forest, range and cropland burning (GALLOWAYet al. 1994). As a nutrient, NOx (NO2-~ + NO3-1) is readily assimilated by phytoplankton and attached plants. This AD-N source has increased most rapidly in developing countries. The dynamics of the generation, transport and fate of these relatively large atmospheric N sources require assessment in the context of managing large scale biogeochemical and trophic impacts. This appears to be a task well-suited for stable isotope analysis. Fortuitously, the isotopic "signature" (5 15N) of dominant N species implicated in atmospheric emission of animal wastes (NH3/NH4 +) and fossil fuel combustion (NOx) are quite distinct (in the case of NH4+ very negative, on the order o f - 7 to -12) from other anthropogenically-generated N sources (i.e. fertilizers, sewage) currently being discharged in surface and groundwater (HEATON 1986). The unique "signature" of atmospherically-derived ammonia/ammonium can serve as a "tracer" of the generation, transport and fate of this important N source (PAERL& FOGEL 1994) (Table 2). In combination with rainfall and
Table 2. Stable nitrogen isotope (5 15N)values (ranges shown) for dominant externally-supplied (new) and internally-supplied (i.e. regenerated) N sources in coastal waters. N Source
~ 15N
N2 in air Remineralized NH4 (estuarine) Sewage Effluent: NH4+ NO3-
0.0 +10.0 to + 16.0 +5.0 to + 11.0 +5.0 to +10.0
Agricultural Land Runoff Fertilizers (Synthetic) Atmospheric Deposition: NH4+ NO3-
+8.0 to + 10.0 -2.0 to +2.0 -13.0 to +2.0 -5.0 to +2.0
References: VELINSKIet al. (1989); FOGEL& CIFUENTES(1993); PAERLet al. (1993). 252
Limnologica 29 (1999) 3
runoff ammonium concentration and loading determinations, we now have the technical capabilities for assessing the butgetary and environmental impacts of these N sources on the ecosystem level.
Groundwater The advent of "modem" agricultural practices, urbanization and industrialization have brought unprecendented use and contamination of groundwater. In coastal regions, relatively shallow aquifers, combined with concentrated human activities, haveput intense pressure on this resource. The use of groundwater for drinking, industrial and agricultural (i.e. irrigation) purposes, combined with ever-increasing applications of synthetic and organic fertilizers, wastes and xenoNotic compounds has led to rapid nutrient enrichment of groundwater. This is especially true for nitrogen, a key component of fertilizers and wastes, whose chemical forms are largely mobile and biologically-reactive. While our understanding of the biogeochemistry of N and other nutrients in groundwater is rudimentary, coastal aquifers residing near anthropogenic N sources reveal varying levels of N contamination, ranging from mM to M concentrations (CAPONE & BAUTISTA 1985; CHURCH 1996). Groundwater N input (into coastal waters) budgets are not well-established; however, this "new" N source can be quantitatively significant (JoHANNES 1980; CAPONE& BAUTISTA1985). Groundwater inputs into the coastal South Atlantic Bight (Georgia-South Carolina) may be equivalent to riverine discharge (MOORE 1996). Clearly, groundwater inputs should be factored into shallow coastal nutrient (especially N) budgets. The relative importance of GW as a source of "new" N is growing. This is particularly true in the coastal agricultural regions of the mid-Atlantic supporting expanding irrigated row-crop, silviculture, livestock and poultry operations. With respect to the latter, coastal North Carolina offers a prime example of groundwater N enrichment from a rapidlyexpanding animal industry. Within half a decade, a significant portion (N25%) of North Carolina's Coastal Plain has been converted from forest and row-crops (corn, soybeans, tobacco) to animal (mostly swine and poultry) operations; a growing percentage of this region's surface area is now covered with animal wastewater lagoons and adjacent fields on which wastes are directly applied as a source of fertilizer. While approximately 1 million production hogs existed in 1990, the current count is approximately 10 million; most are concentrated near the coast. Hogs now outnumber humans by a factor of 2.5. This "explosion" of animals has created a huge waste problem which to date remains largely unresolved. Wastewater lagoons and land-applied waste have been shown to lose substantial amounts of N to groundwater. While land-based animal waste applications are a relatively new phenomenon in the U.S. Atlantic coastal region, this practice has long been in place in Europe's coastal regions (Benelux, France, U.K., Germany, Denmark, Poland).
Recognition of the problem has led to improved management in some regions, with marked reductions in groundwater N contamination. In regions experiencing agricultural economic downtums (Eastern Europe), groundwater N contamination has decreased. Groundwater N contamination continues to be an unabated and growing problem in the U.S. and other agriculturally and industrially "developing" countries. Nitrogen is not be the only accelerating "new" nutrient source to which estuarine and coastal waters exhibit sensitivity. Iron, a variety of trace metals and to a lesser extent phosphorus are also deposited via anthropogenically-enhanced atmospheric and groundwater inputs (CHURCHet al. 1984). Iron additions to some pelagic and coastal oceanic waters are capable of stimulating primary production. Fe and N may interact in a synergistic manner in these waters to enhance primary production (MARTIN et al. 1994; TAKEDAet al. 1995; PAERLet al. 1999) and alter phytoplankton community composition (D~'TuLuo et al. 1993). Fossil fuel combustion, industrial and agricultural emissions, and desertification (as a result of changing land use and vegetation removal) all enhance atmospheric and groundwater Fe and other trace metal emissions and discharges. These hitherto-neglected, but potentially-important, means of stimulating coastal primary production require examination and evaluation. The functional and geographic linkage to accelerating eutrophication and the increased frequency of diverse of phytoplankton blooms should be investigated. Research and management questions addressing this issue include: 1) What are the stoichiometric and functional relationships between externally-supplied "new" nutrient inputs and eutrophication? 2) Is there a functional link between increased "new" nutrient inputs and harmful phytoplankton bloom taxa? 3) Are there unique properties of "new" nutrient sources (N, Fe, trace metals) and combinations thereof, that make them effective agents for supporting harmful blooms and associated water quality degradation (hypoxia, anoxia, toxicity)? 4) What sequences of nutrient loading events are necessary for accelerating eutrophication, initiating and sustaining algal blooms? How do acute and chronic "new" and regenerated loading events translate into enhanced phytoplankton community alterations and bloom formation? 5) What are the relevant spatial (cm, m, kin, 100's of kin, etc.) and temporal (rain, h, d, yr, decades, etc.) scales of nutrient-production interactions we must consider for appropriately assessing, modeling and managing eutrophication dynamics in shallow coastal environments? 6) What roles do synergistic interactions of physical, chemical (nutrient) and biotic (grazing, nutrient regeneration, consortial interactions) factors play in coastal eutrophication dynamics? 7) What microbiological, molecular, analytical and geochemical tools are available and suitable for addressing the above-mentioned research and management questions?
8) How can we best use and integrate existing and evolving remote sensing (aircraft, satellite) technologies to link process research to large scale, synoptic nutrient-production interactions?
What is needed from a coastal research and management perspective? Because ADN and GW represent large and growing sources of "new" N, the dynamics of their formation, transport, deposition and utilization must be clarified and incorporated in management strategies aimed at controlling and reversing cultural eutrophication. Relevant methods, research and management approaches are outlined below. 1) Tools and technologies capable of identifying and tracing local and regional N sources as they impact coastal water quality. Dominant new N inputs exhibit unique stable N isotope (5 15N) "signatures", which may be utilized as tracers. 2) A functional understanding of how new N (and other nutrient) inputs translate into coastal production and food web alterations. Diagnostic plant pigment, physiological and molecular (immunochemical and nucleic acid-based) identification and characterization tools are increasingly-available for this purpose. 3) Complementing technologies with appropriate (i.e. scale and sensitivity) remote sensing and land use characterization (GIS) approaches so that we can we link specific N inputs to coastal biogeochemical and trophic changes. Applications of these technologies will also facilitate regional comparisons of nutrient-production interactions. 4) Determine to what extent nutrient impacts on coastal production are local, regional or global phenomena. 5) Determine the economic and social costs and tradeoffs of water quality management strategies based on the above approaches and resultant criteria.
Acknowledgements: Research support was provided by the National Science Foundation, Projects OCE 9115706, DEB 9210495 and DEB 9220886. Additional support came from the National Sea Grant Office (NOAA), in conjunction with the North Carolina Sea Grant College Program (Projects R/EHP-1, R/MER-23 and R/MER30), and the U.S. Geological Survey/UNC Water Resources Research Institute (Project UNC-790-2). The U.S. Environmental Protection Agency (Air Quality Laboratory, Research Triangle Park, NC) provided atmospheric N deposition data through the regional atmospheric deposition model (RADM).
References ASMAN, W. A. H., HARRISON, R. M. & OTTLEY, C. J. (1994): Estimation of net air-sea flux of ammonia over the southern bight of the North Sea. Atmosph. Environ. 28: 3647-3652.
Limnologica 29 (1999) 3
253
BRIBLECOMBE,P. & STEDMAN,D. H. (1982): Historical evidence for a dramatic increase in the nitrate component of acid rain. Nature 298: 460-462. BUIJSMAN,E., MAAS, H. E M. & ASMAN,W. A. H. (1967): Anthropogenic amonia emissions in Europe. Atmosph. Environ. 21: 1009-1020. CAPONE, D. G. & BAUTISTA,M. E (1985): A groundwater source of nitrate in nearshore marine sediments. Nature 313: 214-216. CHURCH, T. M. (1996): An underground route for the water cycle. Nature 380: 579-580. -- TRAMONTANO,J. M., SCUDLARK,J. e., JICKELLS,T. D., TOKOS,J. J. & KNAPP,A. M. (1984): The wet deposition of trace metals to the western Atlantic Ocean at the mid-Atlantic coast and on Bermuda. Atmosph. Environ. 18: 2657-2664. CODISPOTI, L. A., CHRISTENSEN,J., DEVOL, A., PAERL, H. W. & YOSHINARI, T. (1999): The influence of an unbalanced oceanic combined nitrogen budget on atmospheric carbon dioxide. Mar. Chem. (in press). CORNELL, S., RENDELL,A. & JICKELLS,T. (1995): Atmospheric inputs of dissolved organic nitrogen to the oceans. Nature 376: 243-246. D'ELIA, C. R, SANDERS,J. G. & BOYNTON,W. R. (1986): Nutrient enrichment studies in a coastal plain estuary: phytoplankton growth in large scale, continuous cultures. Can. J. Fish. Aquat. Sci. 43: 397-406. DPTuLLIO, G. R., HUTCHINS,D. A. & BRULAND,K. W. (1993): Interaction of iron and major nutrients controls phytoplankton growth and species composition in the tropical North Pacific Ocean. Limnol. Oceanogr. 38: 495-508. DUCE, R. A. et al. (1991): The atmospheric input of trace species to the world ocean. Global Biogeochem. Cycles 5: 193-259. GALLOWAY,J. N., LEVY II, H. & KASIBAHTLY,P. S. (1994): Year 2020: Consequences of population growth and development on deposition of oxidized nitrogen. Ambio 23: 120-123. GRANELI, E., WALLSTROM,K., LARSSON,U., GRANI~LI,W. & ELMGREN, R. (1990): Nutrient limitation of primary production in the Baltic Sea area. Ambio 19: 142-151. HALLEGRAEEE,G. (1993): A review of harmful algal blooms and their apparent global increase. Phycologia 32: 79-99. HEATON,T. H. E. (1986): Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere. Chem. Geol. 59: 87-102. MARTIN, J. H. et ai. (1994): Testing the iron hypothesis in ecosystems of the equatorial pacific ocean. Nature 371: 123-129. MATSON,E. A. (1993): Nutrient flux through soils and aquifers to the coastal zone of Guam (Mariana Islands). Limnol. Oceanogr. 38: 361-371. MOORE,W. S. (1996): Large groundwater inputs to coastal waters revealed by 226Raenrichments. Nature 380:612-614. NIXON, S. W. (1986): Nutrient dynamics and the productivity of marine coastal waters. In: HALWAGY,R., CLAYTON,D. & BEHBEHANI, M. (eds.), Coastal Eutrophication, pp. 97-115. Oxford. - (1995): Coastal eutrophication: A definition, social causes, and future concerns. Ophelia: 199-220. PAERL,H. W. (1985): Enhancement of marine primary production by nitrogen-enriched acid rain. Nature 315: 747-749.
254
Limnologica 29 (1999) 3
(1988): Nuisance phytoplankton blooms in coastal, estuarine and inland waters. Limnol. Oceanogr. 33: 823-847. - (1993): Emerging role of atmospheric nitrogen deposition in coastal eutrophication: Biogeochemical and trophic perspectives. Can. J. Fish. Aquat. Sci. 50: 2254-2269. - (1997): Coastal eutrophication and harmful algal blooms: importance of atmospheric deposition and groundwater as "new" nitrogen and other nutrient sources. Limnol. Oceanogr. 42:1154-1165. - & FOGEL, M. L. (1994): Isotopic characterization of atmospheric nitrogen inputs as sources of enhanced primary production in coastal Atlantic Ocean waters. Mar. Biol. 119: 635-645. - RUDEK,J. & MALLIN,M. A. (1990): Stimulation of phytoplankton production in coastal waters by natural rainfall inputs: nutritional and trophic implications. Mar. Biol. 107: 247-254. -- MALLIN, M. A., DONMAHUE, C. A., Go, M. & PEIERLS, B. L. (1995): Nitrogen loading sources and eutrophication of the Reuse River estuary, NC: Direct and indirect roles of atmospheric deposition. Report No. 291. Univ. of N. Carolina Water Resources Research Instit., Raleigh, NC, 119 p. - WILLEY, J. D., GO, M., PEIERLS, B. L. & FOGEL, M. L. (1999): Rainfull stimulation of primary production in western Atlantic Ocean waters: roles of different nitrogen sources and co-limiting nutrients. Mar. Ecol. Progr. Ser. 176: 205-214. RIEGMAN, R. (1990): Mechanisms behind eutrophication-induced novel algal blooms. N.I.O.Z. Rapport 9: 1-51. RODHE, H. & ROOD, J. M. (1986): Temporal evolution of nitrogen compounds in Swedish precipitation since 1955. Nature 321: 762-764. RYTHER,J. H. & DUNSTAN,W. M. (1971): Nitrogen, phosphorus and eutrophication in the coastal marine environment. Science 171: 1008-1112. SMETACEK, V., BATHMANN, U., N(~THIG, E.-M. & SCHAREK, R. (1991): Coastal Eutrophication: Causes and consequences. In: MANTOURA,R. C. E, MARTIN,J.-M. & WOLLAST,R. (eds.), Ocean Margin Processes in Global Change, pp. 251-279. Chichester. SOMMER, S. G., CHRISTENSEN,B. T., NIELSEN,N. E. & SCHJORRING, J. K. (1993): Ammonia volatilization during storage of cattle and pig slurry: effect of surface cover. J. Agr. Sci. 121:63-71. TAKEDA,S., KAMATANI,A. & KAWANOBE,K. (1995): Effects of nitrogen and iron enrichments on phytoplankton communities in the northwestern Indian Ocean. Mar. Chem.: 229-241. TIMPERLEY,M. H., VIGOR-BROWN,R. J., KAWASHIMA,M. & ISHIGAMI, D. M. (1985): Organic nitrogen compounds in atmospheric precipitation: their chemistry and availability to phytoplankton. Can. J. Fish. Aquat. Sci. 42: 1171-1177. WOLLAST, R. (1991): The coastal organic carbon cycle: fluxes, sources, and sinks. In: MANTOURA,R. C. E MARTIN, J.-M. & WOLLAST, R. (eds.), Ocean Margin Processes in Global Change, pp. 365-382. Chichester. -
Author's address: HANS W. PAERL, Institute of Marine Sciences, University of North Carolina at Chapel Hill, 3431 Arendell Street, Morehead City, North Carolina, 28557 U.S.A.; Fax: +252/726/2426; e-mail: hpaerl@ email.unc.edu.