Characteristics of Danish Estuaries

Estuaries

Vol. 23, No. 6, p. 820–837

December 2000

Characteristics of Danish Estuaries DANIEL J. CONLEY1,*, HANNE KAAS1,†, FLEMMING MøHLENBERG1,†, BJARKE RASMUSSEN2, and JøRGEN WINDOLF2,‡ 1

Department of Marine Ecology, National Environmental Research Institute, P. O. Box 358, DK4000 Roskilde, Denmark 2 Department of Streams and Riparian Areas, National Environmental Research Institute, P. O. Box 358, DK-4000 Roskilde, Denmark ABSTRACT: We review various aspects of the structure and functioning of Danish estuaries from data collected by the National Monitoring Program and from information in published sources. We present data on the physical, chemical, and biological characteristics of estuaries in Denmark, we evaluate the functioning of these systems as filters and transformers of nutrients, and we evaluate the outlook for Danish estuaries in the future. Danish estuarine systems are for the most part shallow (⬍ 3 m deep), have short residence times, and tend to be heavily loaded with nutrients primarily from agricultural sources. Total average loads from land per unit watershed area are 112 kg P km⫺2 yr⫺1 and 2,400 kg N km⫺2 yr⫺1 during the period 1989–1995. The total phosphorus (TP) load in estuaries has been significantly reduced over the last decade, following implementation of the 1987 Action Plan for the Aquatic Environment (Vandmiljøplan in Danish) that prescribed that nitrogen loads to the total aquatic environment should be reduced by 50% and phosphorus loads by 80%. Reductions in the total nitrogen (TN) load have been more modest. Nutrient loading is one of the primary determinants of estuarine nutrient concentration with 70% of the annual variation in TN concentration and 55% of the annual variation in TP concentration explained by variation in the load. Many Danish estuaries have rich communities of macrophytes and benthic filter feeders, such as Mytlis edulis and Ciona intestinalis, that can control water column chlorophyll concentrations by their filter feeding activities. Many of the estuaries experience hypoxia and anoxia, especially during warm and calm summer months. Further reductions in nutrient loading are expected following implementation of the Action Plan for the Aquatic Environment II, with predicted improvements in oxygen concentrations and in the functioning of these shallow, dynamic estuarine systems.

curred in Denmark during the autumn of 1986 with the report of mass mortality of lobsters caught in fish trawls in the southeastern Kattegat, resulting from widespread distributions of low oxygen concentrations ⬍ 1 ml l⫺1 (Rosenberg et al. 1992). This event captured the attention of the public and solidified the environmental movement in Denmark, stimulating passage of legislation in 1987 by the Danish Parliament (Christensen et al. 1998). This Action Plan on the Aquatic Environment (Vandmiljøplan in Danish) would reduce nitrogen and phosphorus discharges to the total aquatic environment by 50% and 80%, respectively, before 1994 by addressing point and non-point sources of nutrients (Kronvang et al. 1993). A harmonized Aquatic National Monitoring Program was concurrently established to monitor the reduction in nutrient loads (summarized by Kronvang et al. 1993) and to evaluate the ecological effects in the aquatic environment. Data is collected on sources and distribution of nutrients in streams, lakes, and marine waters, in addition to the water quality of groundwater, springs, and point sources from monitoring stations at locations throughout Denmark. Measurements of atmospheric deposition are also made in the program.

Introduction Denmark is endowed with a long coastline (7,300 km) having abundant coastal and estuarine resources. For many centuries, these resources have been intensively used for fisheries, transport, and more recently recreation. The coastal zone has played a particularly important role in the life of the Danish people as a person is no more than 52 km away from the coast anywhere in Denmark. During the long history of varied human exploitation, these resources have been altered and in some instances irrevocably destroyed or seriously degraded. To ensure the sustainable use of Danish estuarine resources, a comprehensive understanding of ecosystem structure and functioning is necessary to manage these systems for future societal demands. Unfortunately an environmental disaster or event (Morris and Bell 1988) is often required to act as a catalyst for society to respond to the degradation of natural resources. Such an event oc* Corresponding author: tele: ⫹45 46 30 12 00; fax: ⫹45 46 30 11 14; e-mail: [email protected]. †Present address: DHI Water and Environment, DK-2730 Hørsholm, Denmark. ‡Present address: County of Funen, Department of Water and Environment, DK-5220 Odense, Denmark. 䊚 2000 Estuarine Research Federation

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Fig. 1. The geographic distribution of estuaries in Denmark. Dotted lines encircle the Limfjorden and Isefjord/Roskilde Fjord complexes. The names corresponding to the estuary number can be found in Table 1.

This monitoring program is one of the most extensive and comprehensive programs in the world, with an emphasis on an integrated approach to studying the aquatic environment. In this paper we review various aspects of the structure and functioning of Danish estuaries from data collected by the National Monitoring Program together with information from published sources. We present data on physical, chemical, and biological characteristics of estuaries in Denmark, evaluate the functioning of these systems as filters and transformers of nutrients, and evaluate the outlook for Danish estuaries in the future. Physical Characteristics For the analysis of Danish estuarine and coastal systems, an estuary was defined as a partially enclosed body of water open to saline water from the

sea and receiving freshwater from rivers, land runoff, or seepage. This broad definition allows for a continuum of different types of estuarine systems (Day et al. 1989). For coastal systems, only bays that were semi-enclosed and meeting the above definition are included in the analysis of Danish estuaries. Geographical data were available for 69 estuaries and chemical and biological data available for 33 estuaries (Fig. 1). Denmark has two large estuarine complexes, e.g., the Limfjord and the Isefjord-Roskilde Fjord complexes, covering areas of c. 1,500 km2 and 420 km2, respectively. By comparison, surface areas for some well studied U.S. estuaries are 11,500 km2 for Chesapeake Bay, 312 km2 for Narragansett Bay, and 28 km2 for Tomales Bay. In the description of Danish estuaries presented here, these large estuarine complexes have been subdivided into their traditional

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TABLE 1. Estuarine codes for estuaries used in the figures. The equivalent English names to the Danish names are: bredning—a broad; bugt—a bay; fjord—defined as an inlet, however it is a broad term used for estuaries and is not to be confused with the classic ‘fjord’ type (although there are classic fjord types such as Mariager Fjord); nor—a cove; sund—a sound or strait; vig—a cove. 1 2 3 4 5 6 7 9 11 17 18 19 20 22 23 24 25 27 28 29 30 31 32 33 34 35 46 49 51 52 53 54 55 57 58 59 60 63 64 65 66 67 68 69 70 71 72 73 74 76 79 81

Roskilde Fjord Karrebæk Fjord Vejle Fjord Horsens Fjord Kolding Fjord Dybsø Fjord Guldborg Sund Nakskov Fjord Stege Bugt Præstø Fjord Nissum Fjord Ringkøbing Fjord Gra˚dyb Tidevandsomra˚de Randers Fjord ˚ rhus Bugt A Norsminde Mariager Fjord Odense Fjord Kertinge Nor/Kerteminde Fjord Det Sydfynske Øhav Holckenhavn Fjord Lindelse Nor Nakkebølle Fjord Helnæs Bugt Bredningen Gamborg Fjord Lunke Bugten Holsteinborg Nor Skælskør Fjord Korsør Nor Kalundborg Fjord Isefjord Yderbredning Lammefjord Inderbredning Holbæk Fjord Hjarbæk Fjord Skive Fjord, Lovns Bredning Flensborg Fjord Haderslev Fjord Aabenraa Fjord Genner Fjord Augustenborg Fjord Nissum Bredning Limfjorden s.f. Mors Limfjorden nv.f. Mors Løgstør Bredning Bjørnholm Bugt/Risga˚rde Bredning Nibe-Gjøl Bredning Limfjorden Sejerø Bugt Køge Bugt

interconnected basins (Fig. 1 and Table 1). We find that 66% of the estuaries are less than 3 m deep and only 6% have average depths greater than 10 m (Fig. 2a). For the most part, they are small, with 43% less than 10 km2 in surface area (Fig. 2b). The watershed areas are not large, with 51% of the es-

Fig. 2. A) Mean depth, B) surface area, C) watershed area, and D) ratio of watershed area to estuary volume for 69 Danish estuaries and their watersheds.

tuaries having a watershed smaller than 100 km2 (Fig. 2c). Nearly two-thirds of Danish estuaries have a ratio of watershed area to estuary volume that exceeds 103 km⫺1 (Fig. 2d). For comparison, the ratio of watershed area to volume of Chesapeake Bay is c. 2,740 km⫺1 and the Bay is considered to be one of the most heavily impacted large marine systems in the world, because of the large watershed area relative to the volume of the estuary (Fig. 1.1 attributed to R. Costanza in Horton and Eichbaum 1991). This comparison suggests that the watershed can have a substantial impact upon these small-volume estuarine systems in Denmark. Freshwater Inputs, Salinity, and Residence Time Although there are no large continental-scale rivers in Denmark, freshwater inputs contribute to the water balance of most Danish coastal systems. In comparison to other rivers on the European continent, the largest river in Denmark ranks only 99 based on annual discharge (Stanners and Bourdeau 1995). Of the rivers with a flow larger than 1 km3 yr⫺1, Gudena˚ (2.6 km3 yr⫺1) is the largest river ˚ emptying into Randers Fjord, followed by Skjern A

Danish Estuaries

Fig. 3.

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Annual mean salinity at stations (⫾ SD) in 47 different Danish estuaries from 1989 to 1995.

(2.3 km3 yr⫺1) draining into Ringkøbing Fjord and Stora˚ (1.1 km3 yr⫺1) draining into Nissum Fjord. Streams, however, are an important component of the Danish landscape (Iversen et al. 1993). The two major salt-water end members for Danish estuaries, both of which can also be considered as estuaries (Gustafsson 2000), vary in salinity from the lower salinity of the Baltic proper (c. 8–9 psu) to the higher North Sea-Skagerrak salinity (c. 32– 34 psu), although most estuaries are connected to the transition area (Kattegat, Øresund, and Belt Seas) between these two sources (Fig. 1). The reported salinity in Danish estuaries will depend upon sampling station location in the estuary and the distance of the station from the freshwater source or from the mouth of the estuary, the salinity of the water body that the estuary connects to, and upon the number of sampling stations that define the mean salinity within a particular estuary. The annual mean salinity and standard deviation of the sampling stations in Danish estuaries shows a board range of spatial and temporal variability (Fig. 3). Spatial differences larger than 10 psu are found in a number of estuaries. Tides are not a significant factor, except along the North Sea coast, e.g., Gra˚dyb Tidevansomra˚de, with the tidal range in Danish estuaries less than c. 20 cm, although water level changes can be large (⬎ 1 m) under the influence of wind. Hydraulic residence times may be estimated in various ways including volume flow arguments, dis-

persion terms, and particle tracing (Officer 1976; Jay et al. 1997). Good agreement has been found between different model types including hydrodynamic, batch-reactor, and morphological models, for estimating water exchange and residence time in Danish estuaries (Rasmussen and Josefson 2000). Sixty-five percent of Danish estuaries have a residence time of ⬍ 0.5 mo, with all estuaries having a residence time of ⬍ 4 mo during winter (Rasmussen and Josefson 2000). We can compare the residence time scales with the flushing time of the estuary by dividing the estuary volume by the freshwater supply. The time scale to flush the estuary is much larger than the residence time with only 29% of estuaries having a flushing time of ⬍ 4 mo and 48% having a flushing time ⬎ 1 yr (Fig. 4). Flushing time is not strongly correlated to the residence time because of mixing with the coastal ocean (Fig. 4) and the flushing time is greatly overestimated in estuaries with small freshwater inputs. While freshwater inputs and the flushing time varies seasonally, decreasing by a factor 4 to 10 during summer, the annual variability in residence time is expected to vary by a factor of 2 (Rasmussen and Josefson 2000). Land Use and Nutrient Loading The geology of Denmark is dominated by Pleistocene tills and fluvio-glacial sedimentary deposits, with predominantly sandy soils in western Denmark and loamy soils in the eastern part of the

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TABLE 2. Population estimates for Denmark. Prehistoric estimates are from Politikens Danmarkshistorie (1985) and modern estimates are from the Statistical Yearbook (1996).

Fig. 4. The flushing time of Danish estuaries calculated by dividing the estuary volume with the freshwater runoff during winter and model calculated adjusted residence time during winter taking into consideration exchange with the coastal ocean (Rasmussen and Josefson 2000).

country. The climate is north temperate with an average annual temperature of 7.7⬚C and 712 mm rainfall annually from 1960 to 1990 (Statistical Yearbook 1996). Anthropogenic changes in Denmark are not a recent phenomena (Bradshaw and Holmqvist 1999) confined to the last several hundred years as in North America, rather it is a cultural landscape that has been systematically altered over the last 6,000 years by human activities (Moe et al. 1989). It is estimated that in 600 AD there were approximately 500,000 people (12 people km⫺2) in Denmark as compared to c. 5.2 million today (Table 2). Through history people have established settlements along the coasts and, therefore, the estuaries are and have been strongly influenced by human activities for a long period of time. The Danish countryside is dominated by intensive farming activities. It is an open landscape characterized by undulating plains with regular plots of arable land termed openfield (Stanners and Bourdeau 1995). Forest cover in Denmark was estimated to be 20% to 25% around 1600 AD with a minimum forest cover of c. 2% to 4% in 1805 (Bradshaw and Holmqvist 1999). A complete statistical compilation of land use has determined that 67% of the land is in agriculture, 12% in forestry, with 10% in urban areas (Statistical Yearbook 1996). By comparison, in 1896 agriculture comprised 76% of the available land area in 1896, forestry with 7%, and urban areas only 2%. It is interesting to note that the dominance of agriculture has remained the most significant landscape feature over the last 100 years. Agricultural production in Denmark is very specialized and highly and consistently productive both per unit land area and per unit re-

Date

Population Estimate

Bronze age (1800–500 BC) Late iron age (AD c. 600) First Census (1769) 1800 1900 1940 1980 1995

c. 200,000 c. 500,000 797,584 929,000 2,432,000 3,844,000 5,123,000 5,233,000

source (Porter and Petersen 1997). Animal husbandry dominates in the western part of the country and plant production (primarily cereals) in the east. In 1995, there were over 11 million pigs produced in Denmark, with 8.5 million in the western peninsula of Jutland (Statistical Yearbook 1996). Although the total number of animals in Danish agriculture has changed little in the last 35 years, there have been large changes in the relative proportions of animals, with large increases in the number of pigs and decreases in poultry and cattle numbers. However, large increases in production have occurred, with a tripling of pig and poultry meat from 1960 to 1994, with changes in agricultural practices in animal husbandry (Porter and Petersen 1997). The variation in N loading from 1989 to 1995 to 47 Danish estuaries has in general followed the variation in freshwater runoff (Fig. 5). The highest TN load per unit of estuarine area was observed in the wet year 1994 ranging from 8.5–52.9 g N m⫺2 yr⫺1 (25th and 75th percentiles), as compared to the dry year of 1989 with the TN load per unit of estuarine area ranging from 4.6–35 g N m⫺2 yr⫺1 (Fig. 5c). The contribution from point sources to TN loading per unit of estuarine area was reduced from 0.7–6.9 g N m⫺2 yr⫺1 in 1989 to 0.62–4.5 g N m⫺2 yr⫺1 in 1995 (25th and 75th percentiles) with improved sewage treatment (Fig. 5b). TN concentrations in the inputs ranged from 414–871 ␮m (25th and 75th percentiles) from 1989 to 1996 with an annual average of 85% of TN in the form of dissolved inorganic nitrogen (Kaas et al. 1996). Area-specific N discharges are among the highest N loads in Europe (Paaby and Møhlenberg 1996), primarily due to the intensity of animal husbandry in Denmark, especially pig farming (Stanners and Bourdeau 1995). The annual area-specific N loading from Denmark average 2,400 kg N km⫺2 yr⫺1 during 1989–1995 (Fig. 5d). By comparison, this loading rate is 1.7 times greater than the areaspecific average N runoff from Northern Europe used to construct N budgets for the North Atlantic at 1,450 kg N km⫺2 yr⫺1 (Howarth et al. 1996).

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Fig. 5. Annual freshwater discharge and nutrient loading to Danish estuaries from 1989 to 1995. A) Freshwater discharge from catchments. B) Total N loading per unit estuary area from sewage outlets in the catchment and direct sewage outfalls to the estuary. C) Total N loading per unit estuary area from rivers and point sources. D) Specific N loading per unit watershed area from rivers and point sources. E) Total P loading per unit estuary area from sewage outlets in the catchment and direct sewage outfalls to the estuary. F) Total P loading per unit estuary area from rivers and point sources. G) Specific P loading per unit watershed area from rivers and point sources. A line is drawn between the annual median. The bars represent the 25th and 75th quartiles and the upper and lower ticks represent the 95th and 5th percentiles, respectively.

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The TN load is dominated by non-point sources attributed to agricultural activities. It has been concluded that N leakage from the root zone in agricultural areas has been reduced by 14% during 1989–1995 due to more environmentally sound farming practices (Kronvang et al. 1999b). The TN load from sewage has been reduced by c. 10,000 tons during 1989–1995, corresponding to a mean specific reduction of 230 kg N km⫺2 on an national basis. The estimated decrease in TN loading is far from the overall national goal of a 50% reduction in N inputs (Kaas et al. 1996). Significant reductions have been observed in P loading with the construction of sewage treatment plants, resulting in a general reduction in the TP load per unit of estuarine area from 0.22–1.8 g P m⫺2 yr⫺1 in 1989 to 0.18–0.84 g P m⫺2 yr⫺1 in 1995 (25th and 75th percentiles) (Fig. 5e). Prior to this period, P loading was dominated by point sources comprising on a national basis c. 90% of the landbased input, whereas point sources presently account for on average only 50% of the P load. Inputs from point sources are easier to identify and control than more diffuse non-point sources and as a result, non-point sources account for a larger share of all inputs more than a decade ago. TP concentrations in freshwater entering the estuaries have been reduced from 8.71–33.6 ␮m in 1989 to 4.19–8.71 ␮m in 1995 (25th and 75th percentiles) with an annual average of 42% of TP in the form of dissolved inorganic phosphate (Kaas et al. 1996). The annual area-specific P load from Denmark averaged 112 kg P km⫺2 yr⫺1 (including direct sewage outfalls) during 1989 to 1995 and was equivalent to the area-specific average specific P runoff from Northern Europe, 117 kg P km⫺2 yr⫺1, used to construct P budgets for the North Atlantic (Howarth et al. 1996). The major part of the seasonal and interannual variation in nitrogen loading to estuaries was related to variations in freshwater discharge (Fig. 6a). In general, both TN and TP loading per unit of estuarine area (Fig. 6c,e) were highest during winter and lowest during summer, analogous to the seasonal variation in freshwater discharge. The concentrations of P in inlets were generally high during the summer period due to less dilution of sewage effluents (Fig. 6d), whereas TN concentrations in inlet waters were generally highest during winter (Fig. 6b) due to high runoff and nutrient leakage from agricultural areas. Other nutrient sources to estuaries include groundwater, the atmosphere, and input from coastal ocean exchange. Although groundwater nutrient concentrations are monitored as part of the National Monitoring Program, there is no information on the magnitude of direct groundwater

inputs into estuarine areas, although they are assumed to be small. The amount of N by atmospheric deposition is measured by the National Monitoring Program and the area-wide N deposition was calculated using the ACDEP (Atmospheric Concentrations and Deposition) model (Hertel et al. 1995). It has been determined that atmospheric N deposition is c. 30% of the TN load to the open waters of the Kattegat (Asman et al. 1995). Because of the small surface area of the estuarine areas and the large load from land, the proportion of N load contributed by the atmosphere is much smaller, with 60% of the estuarine areas receiving less than 10% of their N nutrient input from the atmosphere (Hertel and Frohn 1997). On an area basis, atmospheric N deposition to estuaries ranges from 900–1,000 kg N km⫺2 yr⫺1 (Hertel and Frohn 1997) as compared to the area-specific N loading from land of c. 2,400 kg N km⫺2 yr⫺1, although it is not known how much of the river load originates from direct atmospheric N deposition ( Jaworski et al. 1997). Nutrients also enter Danish estuaries from the coastal ocean, although the influence of the import from the coastal sea is less well known (Kaas et al. 1996). Nutrient Concentrations The seasonal change in the balance between input (loading, sediment remineralization, exchange with open sea) and export (sedimentation, production of biomass, exchange with the open sea, denitrification) gives a characteristic pattern in nutrient concentrations. The median annual concentrations of nutrients in Danish estuaries are 26 ␮m for DIN, 68 ␮m for TN, 0.93 ␮M for DIP, and 2.0 ␮M for TP (Fig. 7). The load of TN and TP is one of the primary determinants of nutrient concentration in Danish estuaries (Table 3) and thus the high loads of nutrients result in relatively high nutrient concentrations in all estuaries. Correlation analyses show that on an annual basis 70% of the variation in TN and 55% of the variation in TP concentrations can be explained by variation in load (Table 3). On a monthly basis, nutrient loading of TN and TP during February was the best predictor of nutrient concentrations explaining 79% and 58% of the estuarine nutrient TN and TP concentrations, respectively. During summer, when freshwater inputs and nutrient loading are low, in situ chemical and biological processes become more important for nutrient concentrations. Thus the lowest correlations between monthly nutrient input and concentrations were observed during summer (Kaas et al. 1996). Nutrient concentrations follow a seasonal pattern (Fig. 8), though deviations occur due to geographical differences (catchment area, topogra-

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Fig. 6. Monthly variation in freshwater discharge, nutrient loading and concentration from 1989 to 1995. A) Freshwater discharge from catchment. B) Inlet concentration of total N from rivers and point sources. C) Total N loading per unit of estuary area from rivers and point sources. D) Inlet concentration of total P from rivers and point sources. E) Total P loading per unit of estuary area from rivers and point sources. A line is drawn between the annual median. The bars represent the 25th and 75th quartiles and the upper and lower ticks represent the 95th and 5th percentiles, respectively.

phy, etc.) and to interannual variations in meteorology (influencing runoff, stratification, and oxygen conditions). During winter, when nutrient loading is high and biological activity low, concentrations of nutrients are correspondingly high. Throughout spring, uptake by primary producers transform N and P nutrients from inorganic to organic forms (Fig. 8c). Concurrent with the decrease in loading, sedimentation of the spring phytoplankton bloom and commencement of macrophyte growth in late spring, nutrient concentrations decrease. DSi (Fig. 8a) and DIP (Fig. 8b) reach minimum concentrations in April, during the peak of the spring bloom; thereafter, regen-

eration in the water column and in particular the sediment exceed uptake, resulting in increasing nutrient concentrations. DSi and DIP concentrations reach their annual maximum during summer because of sediment regeneration, similar to annual cycle patterns observed in other estuarine environments (Conley and Malone 1992; Jensen et al. 1995). DIN concentrations (Fig. 8b) are at a minimum in July–August, and at that time most of the N is bound in particulate matter as TN (Fig. 8c). A significant decrease in phosphorus concentrations has been observed in Danish estuaries due to the 60–70% reduction in TP load from point sources from the mid-1980s to 1996. In 62% of

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Fig. 7. Frequency diagrams of mean annual nutrient concentrations (⫾ SD) in 25 estuaries from 1989 to 1995. A) Dissolved inorganic nitrogen (DIN). B) Total nitrogen (TN). C) Dissolved inorganic phosphate (DIP). D) Total phosphorus (TP).

Danish estuaries, the time-weighted winter (December–March) means of TP and DIP have decreased significantly and in 59% of the estuaries the summer (May–September) DIP level was reduced (Kaas et al. 1996). Sediment-water nutrient fluxes have a significant influence on the nutrient dynamics of Danish estuaries (Lomstien et al. 1998) and are well-studied processes in Denmark (see for example Jørgensen 1983; Fenchel et al. 1998). In addition, bioturbation by benthic fauna has a large influence on the regeneration of organic material in marine sediments (Andersen and Kristensen 1991; Kristensen 1996). Sediment-water nutrient fluxes are also influenced by benthic production of microalgae (Rysgaard et al. 1995) and beds of rooted macrophytes (Risgaard-Petersen et al. 1998). Benthic alTABLE 3. Correlation coefficient between total nitrogen (TN) and total phosphorus (TP) concentrations, and loading in 42 Danish estuaries. All correlations are significant at p ⬍ 0.001. A mean ‘‘nutrient load memory’’ of 2 mo was used as estimated from retention times of the estuaries (Kaas et al. 1996). When more than one measurement was performed within a calendar month, the mean concentration was used. All Months

N-load P-load

February

TN

TP

TN

TP

0.70 0.62

0.49 0.55

0.79 0.78

0.51 0.58

gal mats and ephemeral macroalgae can act as filters for the sediment-water flux of nutrients. A demonstration of the influence of such filters was seen in a small, shallow Danish estuary (Kertinge Nor), where a 6-fold increase in the sediment-water flux of nitrogen was observed from 1991 to 1992, after dense Chaetomorpha linum mats disappeared (Riisga˚rd et al. 1995). The high water column DIP concentrations observed during summer (Fig. 8) arise from sediment regeneration of P, e.g., internal loading. It has been shown that Danish estuaries import P from the open sea during the winter months (Møhlenberg and Ju¨rgensen 1994), store it as Feassociated P in the sediments, and subsequently released as DIP during the warm summer months when aerobic mineralization and sulfate reduction are at their temperature-dependent maximum ( Jensen et al. 1995). Denitrification is an important process in Danish estuaries and can remove a significant portion of the TN load (Rysgaard et al. 1999), although the proportion removed through denitrification is dependent upon the estuarine flushing time (Nielsen et al. 1995; Kaas et al. 1996). Highest denitrification rates are normally found during winter, when nitrate concentrations are at their maximum and good oxygen conditions favor coupled nitrification/denitrification, and denitrification is generally lowest during summer months (Rysgaard et al. 1995).

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Fig. 8. Seasonal variation in nutrient concentrations in 33 estuaries during the period 1989 to 1994. A) Monthly mean concentrations of total nitrogen (TN), total phosphorus (TP), and dissolved silicate (DSi). B) Monthly mean concentration of dissolved inorganic nitrogen (DIN) and dissolved inorganic phosphate (DIP). C) Monthly fraction of total nitrogen that is dissolved inorganic nitrogen (%DIN) and fraction of total phosphorus that is dissolved inorganic phosphate (%DIP).

Nutrient Limitation It is often difficult to pinpoint the limiting nutrient for accumulation of algal biomass in estuaries, due to an array of factors such as morphometry, water movement, light, grazing and loss processes, and nutrient availability, acting alone or in concert. Often much effort is made to find the single limiting factor (Thingstad and Sakshaug 1990), when indeed many factors may act at different spatial and temporal scales (Malone et al. 1996). In addition, estuaries can show shifting patterns of limitation with light limitation during winter, DSi limitation of the spring diatom bloom (Conley and

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Malone 1992), P limitation during the spring, and/ or N limitation during the summer (Conley 1999). Although there is considerable variability in present load characteristics among estuaries and the magnitude of the annual nutrient loadings in 5 shallow estuaries (⬎ 200 g N m⫺2 yr⫺1 and ⬎ 5 g P m⫺2 yr⫺1 of estuarine surface area) makes nutrient limitation in these estuaries unlikely to occur (Kaas et al. 1996). Several studies following the increase in phytoplankton biomass during shortterm enrichment bioassays (Pedersen and Borum 1996) and bioassays using Ulva lactuca (Lyngby and Mortensen 1995) have shown that N is the major limiting nutrient during a major part of the growth season in several Danish estuaries, although P limitation has been observed in early spring (Pedersen and Borum 1996). Additionally, some estuaries, including Hjarbæk Fjord, display strong P limitation throughout the year (Holmboe et al. 1999). Phytoplankton biomass as chlorophyll correlates well with TN concentrations in the water column throughout the growth season, and in particular during summer (Borum 1996). Only during spring does phytoplankton biomass correlate better with TP than with TN. A comparison of chlorophyll concentrations with nutrient loading has shown that phytoplankton biomass correlates more strongly to N load than P load during spring (Pload: r2 ⫽ 0.343; N-load: r2 ⫽ 0.440 for May–June) and during summer (P-load: r2 ⫽ 0.192; N-load: r2 ⫽ 0.421 for July–September) (Kaas et al. 1996). As a result of the gradual increase in tertiary treatment of sewage, the ratio of N:P in land based sources has increased markedly since the 1980s, suggesting that P may become more important in limiting phytoplankton biomass in Danish estuaries in the future. Labile P sources in the sediments are large enough to balance the P deficit in loadings to limit production during summer and autumn in some Danish estuaries ( Jensen and Holmer 1994). There are indications, however, that the period in spring with low DIP concentrations (⬍ 0.1 ␮m) has increased (Kaas et al. 1996). Further reduction may result in P limitation in periods of the growing season as the main decrease is observed in April–May when the water concentrations are already low limiting the spring bloom. Given the high loadings of N and P relative to DSi, the potential for DSi limitation in Danish estuaries is high (Conley and Malone 1992). Potentially limiting concentrations of DSi (⬍ 2 ␮m; Egge and Aksnes 1992) are commonly observed in the open waters surrounding Denmark during the spring and in most of the estuarine systems where DSi data has been collected, including Horsens Fjord, sub-subsystems within the Limfjorden complex, and Ringkøbing Fjord (Dahl et al. 1995).

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Fig. 10. Annual rates of primary production for 33 Danish estuaries from 1989 to 1995.

Fig. 9. Frequency diagram of (A) mean secchi depth (⫾ SD) and (B) mean chlorophyll concentrations (⫾ SD) in 25 estuaries from 1989 to 1995 during the growing season (March– October).

The seasonal cycle of nutrient delivery and uptake can exert strong seasonal patterns in nutrient concentrations, as shown in Fig. 8. Seasonal variations in DIP, DIN, and DSi concentrations and their ratios suggests that many Danish estuaries show shifting patterns of potential nutrient limitation, with DSi limitation of the spring diatom bloom, P limitation also evident during the spring, and strong N limitation throughout the summer. This shifting pattern in nutrient limitation, with DIP limiting during spring and DIN limiting during summer, is a common pattern observed in temperate estuarine systems (Conley 1999). Water Column Chlorophyll and Primary Production The penetration of light as measured by secchi depth, is relatively high in Danish estuaries. A median secchi depth of 3.9 m (Fig. 9a) is observed, although large reductions in light penetration are observed related to wind-induced sediment resuspension (Olesen 1996). Given that 66% of estuaries are shallower than 3 m, a median secchi depth of 3.9 m, means that light availability at the bottom

is sufficient for benthic primary production in many estuaries. The concentration of chlorophyll varies among Danish estuaries (Fig. 9b) and between years as a result of varying nutrient load and grazing control. Mean annual chlorophyll concentration varies between 2 and 50 ␮g l⫺1 with the highest concentrations occurring in the shallowest and most heavily loaded estuaries (Kaas et al. 1996). In a statistical analysis encompassing 25 Danish estuaries and a 6yr period (1989–1995), concentration of chlorophyll was highly correlated to TN load (2.5 mo memory), biomass of benthic grazers (negative), and depth (negative), but only weakly to TP load (Kaas et al. 1996). Depending on seasonal variation in TN load, benthic grazers and depth could explain between 50% and 70% of the observed variation in chlorophyll. Pelagic primary production estimated from 2 h 14 C incubations and calculated for an annual basis varies between 33 and 795 g C m⫺2 yr⫺1 (Fig. 10). The low production rates represents shallow estuaries with low nutrient load (and low chlorophyll concentrations) and high production rates represent areas with high TN load (and high chlorophyll concentration). Oxygen Concentrations It has long been recognized that Danish estuaries encounter problems with anoxia during warm and calm summer months, when density stratification is stable and biological oxygen consumption is at its maximum ( Jørgensen 1980). Prolonged periods of anoxia, in combination with H2S in bottom water, can result in adverse effects on the bottom fauna. In extreme cases, anoxia can also occur throughout the entire water column, affecting pelagic organisms. For example, in August 1997, following a 7-wk period with low winds (⬍ 6 m s⫺1)

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and high temperatures (3–4⬚C above normal), about ⅔ (c. 400,000 tons) of the commercially important population of Mytilus edulis in the Limfjord died and in the inner part of Mariager Fjord all life except protista were killed (Sørensen and Fallesen 1998; Fallesen et al. 2000). Oxygen conditions near the bottom are strongly influenced by vertical mixing processes (Møhlenberg 1999a). In a detailed analysis of oxygen tension in a shallow (c. 4 m) Danish estuary, Skive Fjord, it was possible to separate the effects of physical forcings (buoyancy flux, wind, and solar insolation) and nutrient loadings on oxygen depletion in bottom water. During periods of stratification, the oxygen tension could be described by the time elapsed since the onset of stratification and the accumulated N loading 10 mo prior to a measurement. Using a 10-yr meteorological database, it was then calculated that a 25% reduction in TN loading, half of what was prescribed in the goals of the Action Plan, would reduce the number of days with severe oxygen depletion (i.e., ⬍ 2 mg O2 l⫺1) by 50% (Møhlenberg 1999a). Similar results have been reported for Chesapeake Bay (Cerco 1995), where an evaluation of the effects of hydrodynamics and nutrient loading has determined that hydrodynamics (freshwater flow inducing stratification) is the predominant influence on anoxic volume, although long-term trends in anoxia were also coupled to N loading. Pelagic respiration can also be an important component of oxygen consumption in Danish waters. Jensen et al. (1990) have shown that in Roskilde Fjord, pelagic respiration exceeded benthic respiration and pelagic respiration becomes proportionally larger with increasing eutrophication and phytoplankton productivity in the inner parts of the estuary. These results highlight the importance of phytoplankton blooms for pelagic respiration and overall oxygen balances in Danish estuaries ( Jensen et al. 1990). Occasionally, low oxygen concentrations are caused not just by local processes, but also advective transport of low-oxygen bottom water. For example, intrusions of oxygen-poor water from Kattegat into the estuaries along the eastern coast of Jutland has been reported (Laursen et al. 1992). During time periods of predominantly strong westerly winds saltier, low oxygen bottom water can move from the Kattegat into the estuaries, sometimes creating upwelling of oxygen-poor, nutrientrich water in the inner estuary (Skyum et al. 1994). Pelagic Biology Although studies of phytoplankton taxonomy have a long tradition in Denmark (Ostenfeld 1913), there are only a few systematic investiga-

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tions of phytoplankton species composition in Danish estuaries (Steemann-Nielsen 1951), with most investigations confined to the last 15–20 yr as part of monitoring programs (Kaas et al. 1996). The seasonal succession of the estuarine phytoplankton follows the well-known pattern of temperate waters, with a spring bloom of diatoms in January–March and autumn blooms of dinoflagellates and/or diatoms in September–November. The start of the growth season is determined by ice condition, wind velocity, and irradiance. During winter, biomass is usually low; however in mild sunny, ice-free winters primary production may stay at relatively high levels (Steemann-Nielsen 1951). In harsh winters, spring blooms may occur under the ice, when insulation is high. Algal biomass is usually high throughout summer, and blooms of diatoms, dinoflagellates, and mixotrophic ciliates are common. Nanoflagellates (other than dinoflagellates) only rarely constitute a significant part of the community. The median carbon biomass is 203 ␮g C l⫺1, with most values below 500 ␮g C l⫺1 (Kaas et al. 1996). In many Danish estuaries, the dominant spring diatom is Skeletonema costatum. The mixotrophic ciliate, Mesodinium rubrum, is also very common in the plankton. Although large-cell species dominate the phytoplankton, the biomass of mesozooplankton is low compared to the open waters (Kaas et al. 1996). This suggests that protozoa, rather than mesozooplankton, play a more significant role in the carbon cycling of the water column, and that sedimentation is the major loss process of the larger phytoplankton species (Kiørboe et al. 1994). Concordant with this, tightly coupled oscillations between phytoplankton, heterotrophic flagellates, and ciliates were seen in the Limfjorden estuary (Andersen and Sørensen 1986), and both enclosure and field studies demonstrate the importance of protozoans in estuarine food webs (Riemann et al. 1988; Fenchel et al. 1995). Grazing by blue mussels is probably another determining factor. Blue mussels are widespread in Danish estuaries, and play a major regulatory role for the plankton, including copepod eggs (Møhlenberg 1999b). A general description of the composition and seasonal variation of the zooplankton community can be found in Blanner (1982). An important pelagic predator is the jellyfish Aurelia aurita. The estimated clearance capacity of jellyfish populations shows that A. aurita was capable of filtering the entire water volume in Kertinge Nor several times a day, and that A. aurita was often severely food-limited, rarely exploiting its potential for growth (Olesen et al. 1994; Olesen 1995).

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Benthic Vegetation and Production The large number of shallow estuaries found in Denmark means that light has the capability of reaching the bottom, thus stimulating the growth of both sediment-dwelling microalgae and macrophytes. Indeed rich macrophyte communities can be found in coastal waters. A recent survey of Danish estuaries in 1994 recorded 126 species of macroalgae, 62 belonging to Bangiophyceae, 37 species of Fucophyceae, and 27 species of Chlorophyceae (Middelboe et al. 1998). The most common species of plant is the eelgrass Zostera marina (SandJensen et al. 1994). Many factors interact and regulate the species richness of macroalgae. Middelboe et al. (1998) have shown that species numbers in Danish estuaries increase with salinity, at lower nutrient concentrations, with the availability of hard substrata, and with increased water transparency. The mass wasting of Zostera marina throughout northern Atlantic waters during 1933–1934 was also observed in Denmark (reviewed by Rasmussen 1973), with communities returning to their former abundance by the 1950s. Today, the depth limit of colonization of Zostera marina is correlated to TN concentrations (Sand-Jensen et al. 1994). The depth limit of perennial macrophytes is an indirect function of TN concentration, because of the correlation between phytoplankton biomass and light attenuation in the water column. Reductions in the depth limits of eelgrass observed in Denmark have been attributed to reductions in the light climate (Sand-Jensen et al. 1994). Major deterioration of benthic plant communities have been observed in Danish estuaries (Nielsen et al. 1993), with excessive growths of filamentous algae common. The most studied example is Kertinge Nor (reviewed by Riisga˚rd et al. 1996) where dense mats of Chaetomorpha linum were observed. In other estuaries (Odense Fjord, Roskilde Fjord) dense mats of Ulva lactuca were prevalent (Geertz-Hansen et al. 1993). With reductions in nutrient loading (see above), these excessive growths of filamentous algae have been reduced and are being replaced by seagrasses, such as Zostera and Ruppia. These changes are consistent with prevailing theories concerning the nutrient control of shallow coastal waters regulating the composition of plant communities (Sand-Jensen and Borum 1991; Pedersen and Borum 1996). Primary production by benthic microalgae can also be important in shallow Danish waters (Borum 1996). The shape of the annual primary production cycle can be primarily explained by seasonal changes in temperature and day length (Kristensen 1993). Rapid turnover of organic matter produced by the benthic microalgae has been observed, with c. 30%

of microalgal biomass directly assimilated by benthic grazers (Kristensen 1993). Benthic microalgae strongly regulate the flux of nutrients from or into the sediments, with marked influence on diurnal and seasonal variations in sediment denitrification processes (Rysgaard et al. 1995). Benthic Organisms and Filter Feeders For centuries, the harvesting of oysters dominated the shellfishery of Denmark. Due to a variety of factors, including salinity changes over the last several thousand years, the contribution of oysters has greatly diminished (Kristensen 1997a). Now, the most important commercial shell-fishery in Denmark is for the blue mussel Mytilus edulis. The largest mussel fishery in Danish estuaries occurs in the Limfjorden, averaging over 100,000 tons harvested annually, with the eastern estuaries of Jutland (Kolding Fjord, Vejle Fjord, and Horsens Fjord) contributing c. 25,000 tons annually (Kristensen 1997a). A small mussel fishery (c. 10,000 tons yr⫺1) exists in the Wadden Sea as well (Kristensen 1997b). On average, mollusks, which are dominated by the filter feeding bivalves M. edulis, Mya arenaria, and Cardium spp., comprise 70–90% by weight of the benthic biomass in Danish estuaries (Kaas et al. 1996). The importance of mussels arises from their ability to filter planktonic biomass from the water column (Møhlenberg 1995). In Roskilde Fjord, density stratification can occur during periods of calm weather, with a concomitant increase in phytoplankton biomass. Following windy periods destratification occurs, with decreases in phytoplankton biomass ascribed to filtration by M. edulis, demonstrating the importance of vertical mixing in bringing phytoplankton biomass in contact with the benthic community (Møhlenberg 1995). In a recent review on bivalves in Danish estuaries, Møhlenberg (1999b) has also shown that the filtering capacity of benthic filter feeders varies between 0.02 and 5 estuarine volumes d⫺1 with a median value of 1.2 estuarine volumes d⫺1. The biomass of M. edulis strongly influences the concentrations of chlorophyll in the water column (Fig. 11). Significant negative relationships were found by month from April to September for the period 1989 to 1995 (Kaas et al. 1996). The growth of mussels in Danish estuaries is most often limited by food availability ( Jørgensen 1980), while their distribution is limited by oxygen concentrations (Møhlenberg 1999b). The ascidian, Ciona intestinalis, has also been found to be an important grazer in some Danish waters (Petersen and Riisga˚rd 1992; Riisga˚rd et al. 1995). Although the majority of estuaries are dominated by mollusks, some estuaries are dominated

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Fig. 11. The biomass of mussels and chlorophyll concentrations in April from Danish estuaries with a depth ⬍ 8.5 m from 1989 to 1995.

Fig. 12. Annual rate of primary production by phytoplankton as a function of the rate of input of total nitrogen per unit estuary area. Dashed line is from Fig. 5 in Nixon et al. (1996).

by polychaetes ( Josefson and Rasmussen 2000). The estuaries dominated by polychaetes are either shallow (⬍ 1 m), e.g., Norsminde Fjord, Nissum Fjord, and Halkær Bredning, experience regular resuspension effects, e.g., Ringkøbing Fjord, or suffer periodic anoxia (e.g., Aabenraa Fjord). Burrowing macrofauna such as Arenicola marina, Neries diversicolor, and Hydrobia spp. occupy an important niche along the sandy shallow coastline (Andersen and Kristensen 1991). Further information on distributions and species composition can be found in Thorson (1957), Muus (1967), and Rasmussen (1973), and information on the impact of nutrients on the benthic community can be found in Josefson and Rasmussen (2000).

that previously deposited P in sediments has a significant effect on internal loading of P in many Danish estuaries ( Jensen and Holmer 1994; Kaas et al. 1996). The benthic faunal community has also been shown to retain nutrients as well ( Josefson and Rasmussen 2000), with 25% to 30% of primary production passing through the benthic community. Recent estimates of the overall retention of nutrients in Danish estuaries that empty into the Kattegat suggest that nearly 40% of the watershed TN inputs were retained within the estuarine systems (Ærtebjerg et al. 1998), significantly reducing the annual load to the open waters of the Kattegat. Nutrients also enter Danish estuaries from the coastal waters, although the influence of the import on nutrient mass balances is less well known (Kaas et al. 1996). In the small shallow Kertinge Nor-Kerteminde estuary, measurements and modeling showed a seasonal pattern with net import of P during winter and net export during summer (Møhlenberg and Ju¨rgensen 1994). Chlorophyll concentrations can be strongly correlated to both nutrient concentrations (Sand-Jensen et al. 1994) and nutrient loading (Kaas et al. 1996). However, there was not a significant relationship between the rate of annual primary production in Danish systems compared to the input of TN per unit area (Fig. 12) or to phosphorus (not shown). This is in contrast to the relationship found by Nixon et al. (1996) as indicated by the dashed line in Fig. 12. The important difference in the relationship may be due to the fact that the marine systems used by Nixon et al. (1996) were primarily pelagic dominated systems. Considerable levels of benthic production from both microalgae and macrophytes occur in Danish estuaries (Borum 1996), which may account for this apparent lack of relationship as demonstrated in other estuarine systems.

Danish Estuaries as Filters and Active Transformers of Nutrients Danish estuaries are active transformers of nutrients that convert dissolved inorganic nutrient inputs into algae and aquatic macrophytes, and further into higher trophic levels. Nutrient uptake by the biological systems acts to store nutrients in the estuary during the growing season. Significant abundance of filter feeders, such as blue mussels and other bottom fauna (Worm et al. 2000), significantly reduce concentrations of phytoplankton in the water column (Fig. 11). Although grazing by higher trophic levels regenerates nutrients, some fraction is retained within the estuary. Thus, the biological structure can be an important determinant of the relative size of the sink for nutrients in Danish estuarine systems. The retention of nitrogen in Danish estuarine systems has been found to be dependent upon estuarine residence time (Kaas et al. 1996), consistent with the observations and model of Nixon et al. (1996). However, P is not retained as efficiently in Danish estuaries compared to other estuaries of the world (Kaas et al. 1996). It has been suggested

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Danish Estuaries Are Dynamic, Shallow Systems Phytoplankton productivity and biomass are highly dynamic in estuaries. This is particularly true of shallow, Danish estuaries where biological and physical components are highly coupled (Kamp-Nielsen 1992). Rapid changes in phytoplankton biomass have been observed in Roskilde Fjord triggered by changes in the strength of the physical forcing functions that influence water-column stability and the intensity of vertical mixing and contact with the benthic community (Møhlenberg 1995). During prolonged periods of calm weather and, thus, stability in the water column, phytoplankton populations have the ability to greatly increase their biomass. As water is mixed downward again, for example, following the passage of a weather system, the plankton community once again comes in contact with the high abundance of benthic filter feeders found in these estuaries and the water column is cleared of plankton (Møhlenberg 1999b). Danish estuaries are also prone to occasional periods of anoxia ( Jørgensen 1980). These events can occur both during the summer with oxygen depletion occurring during prolonged periods of water column stability (Sørensen and Fallesen 1998; Møhlenberg 1999a), or during years with severe winters and ice cover (Beukema 1992). Annual variations in the composition of benthic communities can in some areas be regulated by occasional periods of anoxia, creating alternating sequences of extinction and recolonization of benthic communities ( Jørgensen 1980; Rosenberg et al. 1992). These events then have a marked effect on planktonic communities, with higher chlorophyll concentrations occurring during the year following an anoxic event. After reestablishment of benthic communities one or two years later, the system once again is regulated by top-down control of the grazer community. These oscillations in benthic communities have occurred over at least the last 1,000 years in Denmark where written records are available (Hylleberg 1993) or through the use of paleoecological studies of the Danish estuarine environments (Hylleberg 1993). Whether these oscillations can be considered natural occurrences in shallow Danish estuaries, or whether they are due to the long history of human exploitation and eutrophication of coastal waters is not known. Outlook for the Future The nutrient load to Danish waters has been reduced over the last decade by changes in agricultural practices and point source inputs mandated by legislation. Great strides have been made in re-

ducing the TP load to the aquatic environment through better sewage treatment, with only modest reductions in the TN load. Efforts are continuing to further reduce nutrient loadings with additional legislation and implementation of the Vandmiljøplan II (Iversen et al. 1998)—the revised and updated Action Plan for the Aquatic Environment. Therefore, further reductions in nutrient loadings are expected (Kronvang et al. 1999a). New legislation from the Danish Parliament as well as Directives from the Commission of the European Union (EU) are comprehensive, and address nutrient loads by mandating changes in agricultural practices. For example, such changes include setting requirements on maximum livestock units per hectare arable land, construction of storage facilities and specifications on the handling of liquid manure, regulations on application practices and the annual input of fertilizer per hectare of arable land, preparation of fertilizer plans and budgets on each farm, green cover on fields in winter, set-aside of agricultural land, etc. (Bonde 1994; Kronvang et al. 1999a). In addition, improvements are expected in the ecological functioning of streams (Iversen et al. 1993). In the past, most streams experienced extensive regular disturbance including cutting of bank vegetation and clearing of in-stream macrophytes to enhance drainage and the flow of water. As of 1997, that practice has been halted for many streams, and a 2 m buffer strip is now required. The establishment of narrow riparian buffer strips may not be entirely effective however, since nutrients in agricultural runoff often bypass riparian buffers through drainage tiles (Kohl et al. 1971). It is hoped that conversion of readily available inorganic nutrients into organic matter in the streams (macrophytes) and an increase in the efficiency of denitrification with establishment of riparian vegetation (Vought et al. 1994) will enhance the natural ability of streams to process the nutrient loads (Kronvang et al. 1999b). A lag is also expected in the response within Danish estuaries due to the accumulation of internal nutrient pools in estuarine sediments ( Jensen and Holmer 1994). For example, in the small shallow Kertinge Nor-Kerteminde estuary where the major point source, a sewage outfall, has been diverted and the diffuse contribution is low, Christensen et al. (1994) estimated from measurements of the mobile pools and fluxes of N and P that it will take 10 yr for the internal sediment pools to be reduced. Thus, it is hypothesized that the effects of reductions in nutrient loading will be delayed until a lowering of the sediment pools occurs. With the current decline in P loading from improved sewage treatment combined with more or less constant N loading, many estuaries are show-

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ing P limitation, especially during the spring (Conley 1999). Some estuaries, for example Hjarbæk Fjord, are showing P limitation during the entire growing season (Holmboe et al. 1999). Billen and Garnier (1997) hypothesize that P reductions without concomitant reductions in N loading will lead to a greater increase in time periods where P is more limiting than N, especially during spring and the formation of the spring bloom. As N reductions are realized in Danish estuaries, phytoplankton concentrations should be reduced, with increases in the species diversity and in the biomass of benthic vegetation (Sand-Jensen et al. 1994). Although total primary production of shallow areas may remain the same despite predicted reductions in nutrient inputs (Borum and Sand-Jensen 1996), shifts in species composition from fast-growing phytoplankton and ephemeral algae to slow-growing benthic forms should also occur (Sand-Jensen and Borum 1991; Pedersen and Borum 1996). Although Denmark, and Northern Europe in general, was one of the largest contributors per unit of land area to nutrient loads to the aquatic environment (Howarth et al. 1996), significant steps have been taken to reduce nutrient loading and improve the functioning of aquatic ecosystems (Iversen et al. 1998). Denmark’s commitment to reducing nutrient inputs and improving the functioning of ecosystems arises from a national consciousness regarding the environment, and has been strengthened as a result of international agreements, e.g., the Helsinki Commission (HELCOM), the Oslo-Paris Commission (OSPARCOM), and EU agreements. Finally, the expected reductions in nutrient load and the changes that will occur in aquatic ecosystems will be monitored and assessed through the continuing efforts of the Danish National Aquatic Monitoring Program (http:/ www.dmu.dk/). ACKNOWLEDGMENTS We wish to gratefully acknowledge the Danish counties (Amts) who are responsible for data collection for estuaries under the Danish Nationwide Monitoring Program. We wish to express our gratitude for the helpful comments from Peter Bondo Christensen, Annemarie Clarke, Jens Wu¨rgler Hansen, Marianne Holmer, Erik Kristensen, Bente Lomstein, and Bent Odgaard on an earlier version of the manuscript. In addition, we thank the reviewers for their careful attention, which has greatly improved the manuscript. Alf Josefson is thanked for an electronic version of Fig. 1. This paper is a contribution from the IMIS (Integrated Environmental Information Systems) project sponsored by the Danish Environmental Protection Agency.

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UNPUBLISHED MATERIAL

RASMUSSEN, B. AND A. B. JOSEFSON. submitted. Consistent estimates for the residence time of micro-tidal estuaries. Estuarine, Coastal and Shelf Science. Received for consideration, March 1, 1999 Accepted for publication, October 4, 2000