- Email: [email protected]
Nitrogen in Dutch freshwater lakes: trends and targets
ENVIRONMENTAL POLLUTION ELSEVIER
Environmental Pollution 102, Sl (1998) 553-557
Nitrogen in Dutch freshwater lakes: trends and targets D.T. van der Molena*, R. Portieljea, W.T. de Nobelb, P.C.M. Boersa “Institutefor Inland Water Management and Waste Water Treatment, Lelystad, The Netherlands ‘Department of Microbiology, ARISE, University ofAmsterdam, Amsterdam, The Netherlands
Received 27 March 1998; accepted 10 August 1998)
Abstract A trend-analysis
of eutrophication variables revealed that concentrations of total-nitrogen, total-phosphorus and chlorophyll-a decreased over the period 1980-1996 in a large majority of the Dutch freshwater lakes. Relative trends of nutrients compared well with emission reductions, which were much lower for nitrogen compared to phosphorus. Despite the decreasing trends, only 35% of the lakes met the water quality standard for summer mean total-nitrogen of 2.2 mg 1-l. Based on protection against ecological deterioration or possibilities for recovery of eutrophic lakes, a promising goal is a summer mean total-nitrogen of 1.35 mg I-‘. However, atmospheric dinitrogen fixation by blue-green algae will occur in lakes with a growth limiting nitrogen concentration when
sufficient phosphorus, trace metals and light energy are available. Therefore, a combined lake-specific approach of nitrogen and phosphorus emission reduction and top-down control measures may be the best strategy to combat eutrophication. Keywurds:Nitrogen; eutrophication; freshwater lakes; trends; water quality standards
Introduction Since the 1960s programmes have been initiated to reduce nutrient loads to surface waters in order to combat eutrophication effects (e.g. Vollenweider, 1969; Bjork, 1972; Benndorf et al., 1981; Hosper, 1984; Forsberg and Ryding, 1985; Sas, 1989; Jeppesen et al., 1991). Most of these programmes focused on phosphorus (P). Reduction of nitrogen (N) loads have, at most, been carried out parallel with programmes on phosphorus. Sometimes, this focus on P resulted in increased N loads, for example in lakes where phosphate release from sediments was suppressed by nitrate addition (Ripl, 1976; Foy, 1986) and in Lake Veluwe, which was flushed with water rich in nitrate (Hosper, 1984). Nitrogen is considered to be the principal controlling nutrient in coastal areas and open seas (Codispoti, 1989;
* Corresponding author. Tel.: +31-320-298427; fax: +31-320249218; e-mail: [email protected]
Zevenboom, 1994). Recently, the importance of P in controlling primary production of coastal areas and open seas has also been stressed (Peeters and Peperzak, 1990; van Cappellen and Ingall, 1996; Slomp et al., 1996). In freshwaters, P generally is the primary controlling factor in phytoplankton production, but in many aquatic systems N limitation occurs at least for short periods (Sommer, 1989). In this paper we focus on the reduction of N emission in the Netherlands and its effects on the N concentration and phytoplankton in freshwaters. Further, we analyse targets for N in freshwaters, and speculate about the perspectives for N as a controlling factor in managing eutrophication problems.
Trends in eutrophication in Dutch freshwater lakes Initiated by the seventh Rhine Ministers conference (1986, Rotterdam) and the second International Conference on Protection of the North Sea (1987, London),
0.7: van derblolen et al. /Environmental Pollution 102, Sl (1998) 553-557
554
millions
industry domestic wastewater m non-point sources 0
millions
kg N y-’
0
k9 P Y’
250 T
40-r
1975
1980
1985
1990
1992
1995
1975
1980
1985
1990
1992
1995
Fig. 1. Total-N (left) and total-P (right) emissions into Dutch surface freshwaters (Ministerie van Verkeer en Waterstaat, 1981; 1994).
nutrient emissions to surface waters have been reduced in the Netherlands from 1985 to 1995 (Fig. 1). According to the international agreements emissions of both N and P should have been reduced by 50% in 1995 as compared to 1985. The long term goal is a reduction of 70-75% for both N and P. The short term reduction of P emission was already achieved before 1995. In contrast, reduction of N emission was less than 25%. Progress has been made in The Netherlands in the reduction of point sources. Agreements with fertiliser and food industries resulted in lower industrial emissions of P and N, respectively. Non-sewered urban areas have become rare. At the moment, a significant part of the P emission is removed at waste water treatment plants and there are several initiatives to increase N removal as well. Non-point emissions of nutrients have not been reduced and are even expected to increase in the next decades (Boers, 1996; van der Molen et al., 1998). Because lower efforts were put into the reduction of municipal N emission, and non-point emission of N makes up a larger fraction of total emission compared to P, the reduction of N emission is modest compared to the reduction of P emission. However, a trend-analysis of eutrophication variables revealed that in 75% of the lakes in the Netherlands, summer-averaged total-N concentrations decreased over the period 1980-1996 (Portielje and van der Molen, 1998b). In the majority of the lakes negative trends in total-P and chlorophyll-a have also been observed (Table 1). Results for the winter were similar to the results for the summer. These negative trends in the majority of the lakes are consistent with the decrease of the median of the annual distributions in summer mean concentrations of 231 lakes (Table 2). For N, this was even more pronounced in winter (-0.082 mg 1-l year-’ and -2.3% year-’ for the absolute and relative trend respectively), while the decrease in the median of the annual distribution in concentrations of winter mean chlorophyll-a was less obvious (-0.84 pg 1-i year-’ and -1.8% year-‘). These improvements of water quality were observed for
Table 1 Trends in eutrophication variables over 1980-1996 in individual freshwater lakes in the Netherlands (summer means). Significance (atp < 0.1) is expressed as the percentage of the total number of lakes for each variable. Variable
No. of lakes
Total-N
140
Total-P
164
Chlorophyll-a
160
66%
Negative median trend
Significant negative trend
Positive median trend
Significant positive trend
75%
39%
25%
13%
73%
48%
27%
12%
44%
34%
11%
Source: Portielje and van der Molen (1998b). Table 2 Absolute and relative trends in the median of annual summer mean concentrations in Dutch freshwater lakes over 198&1996. Variable
Unit
Absolute trend (year-‘)
Relative trend (% year-‘)
(%)
Total-N
mg 1-l
-0.046
-1.3
22
Total-P
mg 1-t
-0.008
-3.3
56
Chlorophyll-a
mg 1-l
-2.61
-3.6
61
Source: Portielje and van der Molen (1998b).
lakes differing in surface area, average depth or type of sediment. The percentage of lakes with (significant) negative trends is almost comparable for N and P. This is rather surprising given the differences in load reduction for N and P. However, relative trends are much higher for P than for N. In fact, the relative trends expressed as percentage reduction (22% and 56% for N and P, respectively; Table 2,1980-1996) compare very well with the emission reduction achieved for N and P (21% and 56% for N and P, respectively; Fig. 1, 1980-1995). The response time of the P concentration to a load reduction is relatively long in freshwater lakes (Jeppesen et al., 1991; van der Molen and Boers, 1994). The
D. T. van der Molen et aL I EnvinmmentalPollution102, SI (I 998) 553-557
555
time-scale of this delay (up to 16 years according to Jeppesen et al., 1991) is in the same order of magnitude as the period used for the trend-analysis. Due to this long response time, the trends in P concentration are expected to be smaller than those in the emissions. Negative trends in N may partly be explained by negative trends in P. As the amount of nutrients built into suspended organic matter (which generally is a major fraction of both total-P and total-N) is reduced due to P limitation, a larger fraction of the N load will remain dissolved. This fraction is more susceptible to removal by denitrification. This is supported by model calculations for Lake Veluwe, the Netherlands, where the P load decreased and the N load increased since 1979, while both the total-P and total-N concentration decreased significantly (van der Molen et al., 1994). It is hypothesised that a further reduction of N emission does not necessarily lead to a decrease in N concentrations, since a decrease of the amount of N removed by denitrification may counteract the effect of such an emission reduction. For example, Andersen (1977) found a positive correlation between the nitrate concentration in the overlying water and the denitrification rate.
concentration corresponds with maximum concentrations of chlorophyll-a of 55 and 37 pg l-‘, with and without dominance of filamentous blue-green algae respectively. These chlorophyll-a concentrations may allow sufficient light penetration to the sediments, provided no other substances dominate light interception, to facilitate recolonisation of submerged macrophytes in (very) shallow (parts of) lakes, hence allowing ecological recovery. Therefore, a promising goal for protection against ecological deterioration or recovery of stagnant freshwater lakes is a summer mean total-N concentration of 1.35 mg 1-l. In 1996 16% of the Dutch lakes had summer mean total-N concentrations below 1.35 mg I-‘. A comparable level of ecological protection and opportunities for recovery are reached at summer mean concentrations of circa 0.05 mg 1-l total-P, which were found in only 6% of the lakes. If these concentrations are taken as thresholds for growth limitation of blue-green algae, then N limitation occurs more frequently than P limitation in Dutch lakes in recent years.
Water quality standards for nitrogen
Nutrient control is one way to reduce phytoplankton production. Higher trophic levels and macrophytes also affect the relationship between phytoplankton and nutrients. An increased grazing pressure by zooplankton, for example as a result of food web manipulation, decreases maximum chlorophyll-a:nutrient ratios (Portielje and van der Molen, 1998a). In other words, grazing results in a lower maximum chlorophyll-a concentration and, consequently, a higher transparency at a certain nutrient concentration. Decreased maximum chlorophyll-a: nutrient ratios were also found when more than 20% of the lake surface area was covered with submerged macrophytes with a density of more than 15% (Portielje and van der Molen, 1998a). This may be explained by allelopathic effects of macrophytes on phytoplankton (Wium-Andersen et al., 1982) and by the properties of macrophytes as a hiding place to protect zooplankton from predation by fish (Schriver et al., 1995; Lauridsen and Lodge, 1996). These effects of zooplankton and macrophytes indicate top-down control of phytoplankton growth. For submerged macrophytes, bottom-up effects were already observed at 5% coverage of the lake surface area with a density of more than 15% (Portielje and van der Molen, 1998a). Macrophytes cause a decrease in the N concentration, directly, by uptake and, indirectly, by enhancing denitrification via the creation of alternately aerobic and anaerobic zones in the sediment (Carpenter and Lodge, 1986; Caffrey and Kemp, 1992; Rysgaard-Petersen and Jensen, 1997). These processes can be seen as positive feed-backs in lake recovery (Fig. 2).
Apart from emission reductions goals, a water quality standard of 2.2 mg 1-l has been set for the summer mean total-N concentration in stagnant freshwaters in The Netherlands. This standard is based on a maximum chlorophyll-a concentration of 100 pg 1-l and the maximum chlorophyll-a to nutrient ratio in phytoplankton cells. The long term goal is a summer mean total-N concentration of 1.0 mg 1-l (Ministerie van Verkeer en Waterstaat, 1997). The recolonisation of submergent macrophytes is a prerequisite for ecological recovery of freshwater lakes (Carpenter and Lodge, 1986; Coops and Doef, 1996). To achieve this, sufficient light energy at the sediment surface is needed. Analysis of relationships between nutrient and chlorophyll-a concentrations and Secchidisc transparency revealed that the Dutch water quality standard for N is not sufficient for ecological recovery of eutrophic lakes (Portielje and van der Molen, 1998a). Furthermore, the standard for N neither guarantees absence of the nuisance colonial blue-green alga Microcyst~, nor is it sufficient to prevent dominance of filamentous blue-green algae, like Oscillutoriu spp. The standard may be seen as a first step only. In 1996 35% of the lakes met the standard, compared to only 10% in 1980 (Portielje and van der Molen, 1998b). In a data set of 682 lake-years, dominance of both Microcystis and filamentous blue-green algae was not detected below a summer mean concentration of 1.35 mg 1-l total-N (Portielje and van der Molen, 1998a). This N
Perspectives for nitrogen in controlling eutrophication in lakes
556
D. T. van derkfolen et al. I Environmental Pollution 102, Sl (1998) 553-557
transparency
;/
\t
nutrients
--._ -_
,’ --._
---___
,’
__-’
concentration induces comparable ecological effects. Furthermore, reduction of N emission may also be effective when executed for aquatic systems characterised by unfavourable light conditions (e.g. deep lakes or lakes with a high background turbidity) and/or by a relatively high N output (e.g. lakes with a high rate of denitrification or a short hydraulic retention time). An optimum with respect to cost-efficiency of lake recovery may be achieved when lake-specific nutrient programs are combined with lake-specific top-down control measures.
--______-----
Fig. 2. Effect of a reduced nutrient concentration on phytoplankton and feed-backs on phytoplankton via macrophytes and zooplankton and on nutrients by macrophytes.
Direct measurement of denitrification rates is still laborious and erroneous, and as a consequence a wide range of different methods is used (Seitzinger et al., 1993; van Luijn et al., 1996; Middelburg et al., 1996). In general, knowledge on retention of N and on effects of organic matter on the denitrification process is still partial. Denitrification may be coupled with primary production, with lower removal rates at both high and low production of organic matter (Berge et al., 1997; van Luijn et al., 1998). Organic matter is needed for the reduction of nitrate to dinitrogen (N,), but too much organic matter may exhaust oxygen and therefore hamper the oxidation of ammonium to nitrate. Denitrification of nitrate may lower the N:P ratio in the sediment, and ultimately N may become the limiting factor for phytoplankton growth in the overlying water. Contrary to the export of N from ecosystems in gaseous form by denitrification, several blue-green algae are able to use atmospheric N, for primary production. If the other essential resources (e.g. P, trace metals and light energy) are in ample supply, growth limiting N concentrations will trigger the development of N2-fixing blue-green algal blooms (Paerl, 1990). A shortage of light energy or P is known to hamper the growth of N,-fixing blue-greens (Zevenboom and Mur, 1980; de Nobel, 1998). N, fixing blue-green algae produce less biomass per unit of P and become limited by P at a higher concentration of dissolved P compared to non-N, fixing algae (de Nobel et al., 1997). Based on an extensive data set, dominance of N,fixing blue-green algae was found to occur only very rarely in Dutch freshwater lakes (Portielje and van der Molen, 1998a). However, since the N input by N, fmation can be significant (Howarth et al., 1988; de Nobel, 1998), a general program of N emission reduction may not be very cost-effective. On the other hand, a program based on P solely is costly, especially a further reduction of a low P load to a very low P load. Compared to an approach exclusively based on reduction of P emissions, the reduction of the P concentration may not have to be so excessive if a combination with reduction of the N
Conclusions The negative relative trends in N and P concentrations in Dutch freshwater lakes correspond to the emission reductions, which are less for N compared to P. However, further reduction of N emission may have less effect on the N concentrations, since removal of dissolved N by denitrification may decrease as well. The N concentrations in most lakes in the Netherlands have decreased, but only in a small percentage of the lakes they met the Dutch water quality standard of 2.2 mg 1-l total-N (summer mean). This water quality standard for total-N is still too high to prevent dominance of blue-green algae, and will not be sufficient to initiate ecological recovery by recolonisation of submerged macrophytes in shallow lakes. Therefore, the water quality standard should be reduced to 1.35 mg 1-l total-N. Increased grazing pressure by zooplankton and recolonisation of submerged macrophytes negatively affect the phytoplankton biomass. - There is little risk for appearance of N,-fixing bluegreen algae if apart from the N concentration the P concentration is sufficiently low as well. A combined program of N and P emission reduction and top-down control measures in a lake-specific approach, may further improve the water quality in Dutch freshwater lakes.
References Andersen, J.M., 1977. Rates of denitrification of undisturbed sediment from six lakes as a function of nitrate concentration, oxygen and temperature. Archiv fur Hydrobiologie 80,147-159. Benndorf, J., Uhhnann, D., Piitz, K., 1981. Strategies for water quality management in reservoirs in the German Democratic republic. Water Quality Bulletin 6,68-73. Berge, D., Fjeld, E., Hindar, A., Kaste, O., 1997. Nitrogen retention in two Norwegian watercourses of different trophic status. Ambio 26, 282-288. Bjork, S., 1972. Swedish lake restoration program gets results. Ambio 1, 153-165. Boers, P.C.M., 1996. Nutrient emissions from agriculture in The Netherlands, causes and remedies. Water Science and Technology 33, 183-189.
D.T. van der Molen et al. I Environmental Pollution 102, Sl (1998) 553-557
Caffrey, J.M., Kemp, M., 1992. Influence of the submersed plant, Potamogetonperfoliatus, on nitrogen cycling in estuarine sediments. Limnology and Oceanography 37,1483-1495. Carpenter, S.R., Lodge, D.M., 1986. Effects of submersed macrophytes on ecosystem processes. Aquatic Botany 26,341-370. Codispoti, L.A., 1989. Phosphorus vs. Nitrogen limitation of new and export production. In: W.H. Berger, V.S. Smetacek and G. Wefer (Eds.), Productivity of the Oceans, Present and Past. Wiley, New York, pp. 377-394. Coops, H., Doef, R.W., 1996. Submerged vegetation development in two shallow, eutrophic lakes. Hydrobiologia 340,115-120. De Nobel, W.T., 1998. Ecophysiology of the nitrogen-fixing cyanobacteria Anabaena and Aphanizomenon in relation to eutrophication. Ph.D. thesis, University of Amsterdam, The Netherlands. 99 PP. De Nobel, W.T., Snoep, J.L., Westerhoff, H.V., Mur, L.R., 1997. Interaction of nitrogen furation and phosphorus limitation in Aphanizomenon flos-aquae (Cyanophyceae). Journal of Phycology 33, 794-799. Forsberg, C., Ryding, S.-O., 1985. Research on recovery of polluted lakes. Hur tillfrisknade sjoarna? Vatten 41,3-19 (in Swedish). Foy, R.H., 1986. Suppression of phosphorus release from lake sediments by the addition of nitrate. Water Research 20,1345-1351. Hosper, S.H. (1984) Restoration of Lake Veluwe, The Netherlands, by reduction of phosphorus loading and flushing. Water Science and Technology 17,757-768. Howarth, R.W., Marino, R., Lane, J., Cole, J.J., 1988. Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance. Limnology and Oceanography 33,669-687. Jeppesen, E., Kristensen, P., Jensen, J.P., Sondergaard, M., Mortensen, E., Lauridsen, T., 1991. Recovery resilience following a reduction in external phosphorus loading of shallow, eutrophic Danish lakes: duration, regulating factors and methods for overcoming resilience. Memorie dell’Istituto Italiano di Idrobiologia 48, 127-148. Lauridsen, T.L., Lodge, D.M., 1996. Avoidance by Daphnia magna of fish and macrophytes: chemical cues and predator mediated use of macrophyte habitat. Limnology and Oceanography 41,794-798. Middelburg, J.J., Soetaert, K., Herman, P.M.J., 1996. Evaluation of the nitrogen isotope-pairing method for measuring benthic denitrification: a simulation analysis. Limnology and Oceanography 41, 1839-1844. Ministerie van Verkeer en Waterstaat, 1981. Indicative Water Program 1980-1984. Indicatief Meerjarenprogramma Water 1980-1984. Staatsuitgeverij, ‘s-Gravenhage, ISBN 9012032717 (in Dutch). Ministerie van Verkeer en Waterstaat, 1994. Water in The Netherlands: a time for action. (Water voor Nu en Later.) Voortgangsrapportage Integraal Waterbeheer en Noordzee-aangelegenheden 1994 (in Dutch). Ministerie van Verkeer en Waterstaat, 1997. The Fourth National Policy Document on Watermanagement. Vierde Nota waterhuishouding. Regeringsvoomemen. ISBN 9039913560 (in Dutch). Paerl, H.W., 1990. Physiological ecology and regulation of N, fixation in natural waters. Advances in Microbial Ecology 11,305-344. Peeters, J.C.H., Peperzak, L., 1990. Nutrient limitation in the North Sea: a bioassay approach. Netherlands Journal of Sea Research 26, 61-73. Portielje, R., van der Molen, D.T., 1998a. Relationships between eutrophication variables and system properties in Dutch freshwater lakes. Relaties tussen eutrofilringsvariabelen en systeem-
557
kenmerken van de Nederlandse meren en plassen. Deelrapport II voor de Vierde Eutrofieringsenquete. RIZA rapport 98.007, Lelystad. ISBN 9036951585 (in Dutch). Portielje, R., van der Molen, D.T., 1998b. Trend-analysis of eutrophication variables in lakes in The Netherlands. Water Science and Technology 37,235-240. Ripl, W., 1976. Biochemical oxidation of polluted lake sediment with nitrate -a new lake restoration method. Ambio 5, 132-135. Rysgaard-Petersen, N., Jensen, K., 1997. Nitrification and denitrification in the rhizosphere of the aquatic macrophyte Lobelia dortmanna L. Limnology and Oceanography 42,529-537. Sas, H., 1989. Lake Restoration by Reduction of Nutrient Loading: Expectations, Experiences, Extrapolations. Academia Verlag Richarz GmbH, St. Augustin. ISBN 388345379 X. 497 pp. Schriver, P., Bogestrand, J., Jeppesen, E., Sondergaard, M., 1995. Imact of submerged macrophytes on fish-zooplankton-phytoplankton interactions: large-scale enclosure experiments in a shallow eutrophic lake. Freshwater Biology 33,255-270. Seitzinger, S.P., Nielsen, L.P., Caffrey, J., Christensen, P.B., 1993. Denitrification measurements in aquatic sediments: a comparison of three methods. Biochemistry 23,147-167. Slomp, C.P., van der Gaast, S.J., and van Raaphorst, W., 1996. Phosphorus binding by poorly cristalline iron oxides in North Sea sediments. Marine Chemistry 52,55-73. Sommer, U., 1989. Nutrient status and nutrient competition of phytoplankton in a shallow, hypertrophic lake. Limnology and Oceanography 34,1162-1173. Van Cappellen, P., Ingall, E.D., 1996. Redox stabilization of the atmosphere and oceans by phosphorus-limited marine productivity. Science 27l493-496. Van der Molen, D.T., Boers, P.C.M., 1994. Influence of internal loading on phosphorus concentration in shallow lakes before and after reduction of the external loading. Hydrobiologia 275/276,379-389. Van der Molen, D.T., Boers, P.C.M., Breeuwsma, A., 1998. Agricultural nutrient losses to surface waters in the Netherlands: impact, strategies and perspectives. Journal of Environmental Quality 27, 4-11. Van der Molen, D.T., Los, F.J., van Ballegooijen L., van der Vat, M.P., 1994. Mathematical modelling as a tool for management in eutrophication control of shallow lakes. Hydrobiologia 275/276,479-492. Van Luijn, F., Boers, P.C.M., LijkIema, L., 1996. Comparison of denitrification rates obtained by the N, flux method, the 15N isotope pairing technique and the mass balance approach. Water Research 30,893~900. Van Luijn, F., Boers, P.C.M., LijkIema, L., Sweerts, J.-P.R.A., 1998. Nitrogen fluxes and processes in sandy and muddy sediments from a shallow eutrophic lake. Water Research, in press. Vollenweider, R.A., 1969. Moglichkeiten und Grenzen elementarer Modelle der Stoftbilanz von Seen. Archiv fiir Hydrobiologie 66, l-36 (in German). Wium-Andersen, S., Anthoni, U., Christophersen, C., Houen, G., 1982. Allelopathic effects on phytoplankton by substances isolated from aquatic macrophytes (Charales). Oikos 39, 187-190. Zevenboom, W., 1994. Assessment of eutrophication and its effects in marine waters. German Journal of Hydrography, Supplement 1, 141-170. Zevenboom, W. and Mur, L.R., 1980. N,-fixing cyanobacteria: why they do not become dominant in Dutch, hypertrophic lakes. Developments in Hydrobiology 2,123-130.
Environmental Pollution 102, Sl (1998) 553-557
Nitrogen in Dutch freshwater lakes: trends and targets D.T. van der Molena*, R. Portieljea, W.T. de Nobelb, P.C.M. Boersa “Institutefor Inland Water Management and Waste Water Treatment, Lelystad, The Netherlands ‘Department of Microbiology, ARISE, University ofAmsterdam, Amsterdam, The Netherlands
Received 27 March 1998; accepted 10 August 1998)
Abstract A trend-analysis
of eutrophication variables revealed that concentrations of total-nitrogen, total-phosphorus and chlorophyll-a decreased over the period 1980-1996 in a large majority of the Dutch freshwater lakes. Relative trends of nutrients compared well with emission reductions, which were much lower for nitrogen compared to phosphorus. Despite the decreasing trends, only 35% of the lakes met the water quality standard for summer mean total-nitrogen of 2.2 mg 1-l. Based on protection against ecological deterioration or possibilities for recovery of eutrophic lakes, a promising goal is a summer mean total-nitrogen of 1.35 mg I-‘. However, atmospheric dinitrogen fixation by blue-green algae will occur in lakes with a growth limiting nitrogen concentration when
sufficient phosphorus, trace metals and light energy are available. Therefore, a combined lake-specific approach of nitrogen and phosphorus emission reduction and top-down control measures may be the best strategy to combat eutrophication. Keywurds:Nitrogen; eutrophication; freshwater lakes; trends; water quality standards
Introduction Since the 1960s programmes have been initiated to reduce nutrient loads to surface waters in order to combat eutrophication effects (e.g. Vollenweider, 1969; Bjork, 1972; Benndorf et al., 1981; Hosper, 1984; Forsberg and Ryding, 1985; Sas, 1989; Jeppesen et al., 1991). Most of these programmes focused on phosphorus (P). Reduction of nitrogen (N) loads have, at most, been carried out parallel with programmes on phosphorus. Sometimes, this focus on P resulted in increased N loads, for example in lakes where phosphate release from sediments was suppressed by nitrate addition (Ripl, 1976; Foy, 1986) and in Lake Veluwe, which was flushed with water rich in nitrate (Hosper, 1984). Nitrogen is considered to be the principal controlling nutrient in coastal areas and open seas (Codispoti, 1989;
* Corresponding author. Tel.: +31-320-298427; fax: +31-320249218; e-mail: [email protected]
Zevenboom, 1994). Recently, the importance of P in controlling primary production of coastal areas and open seas has also been stressed (Peeters and Peperzak, 1990; van Cappellen and Ingall, 1996; Slomp et al., 1996). In freshwaters, P generally is the primary controlling factor in phytoplankton production, but in many aquatic systems N limitation occurs at least for short periods (Sommer, 1989). In this paper we focus on the reduction of N emission in the Netherlands and its effects on the N concentration and phytoplankton in freshwaters. Further, we analyse targets for N in freshwaters, and speculate about the perspectives for N as a controlling factor in managing eutrophication problems.
Trends in eutrophication in Dutch freshwater lakes Initiated by the seventh Rhine Ministers conference (1986, Rotterdam) and the second International Conference on Protection of the North Sea (1987, London),
0.7: van derblolen et al. /Environmental Pollution 102, Sl (1998) 553-557
554
millions
industry domestic wastewater m non-point sources 0
millions
kg N y-’
0
k9 P Y’
250 T
40-r
1975
1980
1985
1990
1992
1995
1975
1980
1985
1990
1992
1995
Fig. 1. Total-N (left) and total-P (right) emissions into Dutch surface freshwaters (Ministerie van Verkeer en Waterstaat, 1981; 1994).
nutrient emissions to surface waters have been reduced in the Netherlands from 1985 to 1995 (Fig. 1). According to the international agreements emissions of both N and P should have been reduced by 50% in 1995 as compared to 1985. The long term goal is a reduction of 70-75% for both N and P. The short term reduction of P emission was already achieved before 1995. In contrast, reduction of N emission was less than 25%. Progress has been made in The Netherlands in the reduction of point sources. Agreements with fertiliser and food industries resulted in lower industrial emissions of P and N, respectively. Non-sewered urban areas have become rare. At the moment, a significant part of the P emission is removed at waste water treatment plants and there are several initiatives to increase N removal as well. Non-point emissions of nutrients have not been reduced and are even expected to increase in the next decades (Boers, 1996; van der Molen et al., 1998). Because lower efforts were put into the reduction of municipal N emission, and non-point emission of N makes up a larger fraction of total emission compared to P, the reduction of N emission is modest compared to the reduction of P emission. However, a trend-analysis of eutrophication variables revealed that in 75% of the lakes in the Netherlands, summer-averaged total-N concentrations decreased over the period 1980-1996 (Portielje and van der Molen, 1998b). In the majority of the lakes negative trends in total-P and chlorophyll-a have also been observed (Table 1). Results for the winter were similar to the results for the summer. These negative trends in the majority of the lakes are consistent with the decrease of the median of the annual distributions in summer mean concentrations of 231 lakes (Table 2). For N, this was even more pronounced in winter (-0.082 mg 1-l year-’ and -2.3% year-’ for the absolute and relative trend respectively), while the decrease in the median of the annual distribution in concentrations of winter mean chlorophyll-a was less obvious (-0.84 pg 1-i year-’ and -1.8% year-‘). These improvements of water quality were observed for
Table 1 Trends in eutrophication variables over 1980-1996 in individual freshwater lakes in the Netherlands (summer means). Significance (atp < 0.1) is expressed as the percentage of the total number of lakes for each variable. Variable
No. of lakes
Total-N
140
Total-P
164
Chlorophyll-a
160
66%
Negative median trend
Significant negative trend
Positive median trend
Significant positive trend
75%
39%
25%
13%
73%
48%
27%
12%
44%
34%
11%
Source: Portielje and van der Molen (1998b). Table 2 Absolute and relative trends in the median of annual summer mean concentrations in Dutch freshwater lakes over 198&1996. Variable
Unit
Absolute trend (year-‘)
Relative trend (% year-‘)
(%)
Total-N
mg 1-l
-0.046
-1.3
22
Total-P
mg 1-t
-0.008
-3.3
56
Chlorophyll-a
mg 1-l
-2.61
-3.6
61
Source: Portielje and van der Molen (1998b).
lakes differing in surface area, average depth or type of sediment. The percentage of lakes with (significant) negative trends is almost comparable for N and P. This is rather surprising given the differences in load reduction for N and P. However, relative trends are much higher for P than for N. In fact, the relative trends expressed as percentage reduction (22% and 56% for N and P, respectively; Table 2,1980-1996) compare very well with the emission reduction achieved for N and P (21% and 56% for N and P, respectively; Fig. 1, 1980-1995). The response time of the P concentration to a load reduction is relatively long in freshwater lakes (Jeppesen et al., 1991; van der Molen and Boers, 1994). The
D. T. van der Molen et aL I EnvinmmentalPollution102, SI (I 998) 553-557
555
time-scale of this delay (up to 16 years according to Jeppesen et al., 1991) is in the same order of magnitude as the period used for the trend-analysis. Due to this long response time, the trends in P concentration are expected to be smaller than those in the emissions. Negative trends in N may partly be explained by negative trends in P. As the amount of nutrients built into suspended organic matter (which generally is a major fraction of both total-P and total-N) is reduced due to P limitation, a larger fraction of the N load will remain dissolved. This fraction is more susceptible to removal by denitrification. This is supported by model calculations for Lake Veluwe, the Netherlands, where the P load decreased and the N load increased since 1979, while both the total-P and total-N concentration decreased significantly (van der Molen et al., 1994). It is hypothesised that a further reduction of N emission does not necessarily lead to a decrease in N concentrations, since a decrease of the amount of N removed by denitrification may counteract the effect of such an emission reduction. For example, Andersen (1977) found a positive correlation between the nitrate concentration in the overlying water and the denitrification rate.
concentration corresponds with maximum concentrations of chlorophyll-a of 55 and 37 pg l-‘, with and without dominance of filamentous blue-green algae respectively. These chlorophyll-a concentrations may allow sufficient light penetration to the sediments, provided no other substances dominate light interception, to facilitate recolonisation of submerged macrophytes in (very) shallow (parts of) lakes, hence allowing ecological recovery. Therefore, a promising goal for protection against ecological deterioration or recovery of stagnant freshwater lakes is a summer mean total-N concentration of 1.35 mg 1-l. In 1996 16% of the Dutch lakes had summer mean total-N concentrations below 1.35 mg I-‘. A comparable level of ecological protection and opportunities for recovery are reached at summer mean concentrations of circa 0.05 mg 1-l total-P, which were found in only 6% of the lakes. If these concentrations are taken as thresholds for growth limitation of blue-green algae, then N limitation occurs more frequently than P limitation in Dutch lakes in recent years.
Water quality standards for nitrogen
Nutrient control is one way to reduce phytoplankton production. Higher trophic levels and macrophytes also affect the relationship between phytoplankton and nutrients. An increased grazing pressure by zooplankton, for example as a result of food web manipulation, decreases maximum chlorophyll-a:nutrient ratios (Portielje and van der Molen, 1998a). In other words, grazing results in a lower maximum chlorophyll-a concentration and, consequently, a higher transparency at a certain nutrient concentration. Decreased maximum chlorophyll-a: nutrient ratios were also found when more than 20% of the lake surface area was covered with submerged macrophytes with a density of more than 15% (Portielje and van der Molen, 1998a). This may be explained by allelopathic effects of macrophytes on phytoplankton (Wium-Andersen et al., 1982) and by the properties of macrophytes as a hiding place to protect zooplankton from predation by fish (Schriver et al., 1995; Lauridsen and Lodge, 1996). These effects of zooplankton and macrophytes indicate top-down control of phytoplankton growth. For submerged macrophytes, bottom-up effects were already observed at 5% coverage of the lake surface area with a density of more than 15% (Portielje and van der Molen, 1998a). Macrophytes cause a decrease in the N concentration, directly, by uptake and, indirectly, by enhancing denitrification via the creation of alternately aerobic and anaerobic zones in the sediment (Carpenter and Lodge, 1986; Caffrey and Kemp, 1992; Rysgaard-Petersen and Jensen, 1997). These processes can be seen as positive feed-backs in lake recovery (Fig. 2).
Apart from emission reductions goals, a water quality standard of 2.2 mg 1-l has been set for the summer mean total-N concentration in stagnant freshwaters in The Netherlands. This standard is based on a maximum chlorophyll-a concentration of 100 pg 1-l and the maximum chlorophyll-a to nutrient ratio in phytoplankton cells. The long term goal is a summer mean total-N concentration of 1.0 mg 1-l (Ministerie van Verkeer en Waterstaat, 1997). The recolonisation of submergent macrophytes is a prerequisite for ecological recovery of freshwater lakes (Carpenter and Lodge, 1986; Coops and Doef, 1996). To achieve this, sufficient light energy at the sediment surface is needed. Analysis of relationships between nutrient and chlorophyll-a concentrations and Secchidisc transparency revealed that the Dutch water quality standard for N is not sufficient for ecological recovery of eutrophic lakes (Portielje and van der Molen, 1998a). Furthermore, the standard for N neither guarantees absence of the nuisance colonial blue-green alga Microcyst~, nor is it sufficient to prevent dominance of filamentous blue-green algae, like Oscillutoriu spp. The standard may be seen as a first step only. In 1996 35% of the lakes met the standard, compared to only 10% in 1980 (Portielje and van der Molen, 1998b). In a data set of 682 lake-years, dominance of both Microcystis and filamentous blue-green algae was not detected below a summer mean concentration of 1.35 mg 1-l total-N (Portielje and van der Molen, 1998a). This N
Perspectives for nitrogen in controlling eutrophication in lakes
556
D. T. van derkfolen et al. I Environmental Pollution 102, Sl (1998) 553-557
transparency
;/
\t
nutrients
--._ -_
,’ --._
---___
,’
__-’
concentration induces comparable ecological effects. Furthermore, reduction of N emission may also be effective when executed for aquatic systems characterised by unfavourable light conditions (e.g. deep lakes or lakes with a high background turbidity) and/or by a relatively high N output (e.g. lakes with a high rate of denitrification or a short hydraulic retention time). An optimum with respect to cost-efficiency of lake recovery may be achieved when lake-specific nutrient programs are combined with lake-specific top-down control measures.
--______-----
Fig. 2. Effect of a reduced nutrient concentration on phytoplankton and feed-backs on phytoplankton via macrophytes and zooplankton and on nutrients by macrophytes.
Direct measurement of denitrification rates is still laborious and erroneous, and as a consequence a wide range of different methods is used (Seitzinger et al., 1993; van Luijn et al., 1996; Middelburg et al., 1996). In general, knowledge on retention of N and on effects of organic matter on the denitrification process is still partial. Denitrification may be coupled with primary production, with lower removal rates at both high and low production of organic matter (Berge et al., 1997; van Luijn et al., 1998). Organic matter is needed for the reduction of nitrate to dinitrogen (N,), but too much organic matter may exhaust oxygen and therefore hamper the oxidation of ammonium to nitrate. Denitrification of nitrate may lower the N:P ratio in the sediment, and ultimately N may become the limiting factor for phytoplankton growth in the overlying water. Contrary to the export of N from ecosystems in gaseous form by denitrification, several blue-green algae are able to use atmospheric N, for primary production. If the other essential resources (e.g. P, trace metals and light energy) are in ample supply, growth limiting N concentrations will trigger the development of N2-fixing blue-green algal blooms (Paerl, 1990). A shortage of light energy or P is known to hamper the growth of N,-fixing blue-greens (Zevenboom and Mur, 1980; de Nobel, 1998). N, fixing blue-green algae produce less biomass per unit of P and become limited by P at a higher concentration of dissolved P compared to non-N, fixing algae (de Nobel et al., 1997). Based on an extensive data set, dominance of N,fixing blue-green algae was found to occur only very rarely in Dutch freshwater lakes (Portielje and van der Molen, 1998a). However, since the N input by N, fmation can be significant (Howarth et al., 1988; de Nobel, 1998), a general program of N emission reduction may not be very cost-effective. On the other hand, a program based on P solely is costly, especially a further reduction of a low P load to a very low P load. Compared to an approach exclusively based on reduction of P emissions, the reduction of the P concentration may not have to be so excessive if a combination with reduction of the N
Conclusions The negative relative trends in N and P concentrations in Dutch freshwater lakes correspond to the emission reductions, which are less for N compared to P. However, further reduction of N emission may have less effect on the N concentrations, since removal of dissolved N by denitrification may decrease as well. The N concentrations in most lakes in the Netherlands have decreased, but only in a small percentage of the lakes they met the Dutch water quality standard of 2.2 mg 1-l total-N (summer mean). This water quality standard for total-N is still too high to prevent dominance of blue-green algae, and will not be sufficient to initiate ecological recovery by recolonisation of submerged macrophytes in shallow lakes. Therefore, the water quality standard should be reduced to 1.35 mg 1-l total-N. Increased grazing pressure by zooplankton and recolonisation of submerged macrophytes negatively affect the phytoplankton biomass. - There is little risk for appearance of N,-fixing bluegreen algae if apart from the N concentration the P concentration is sufficiently low as well. A combined program of N and P emission reduction and top-down control measures in a lake-specific approach, may further improve the water quality in Dutch freshwater lakes.
References Andersen, J.M., 1977. Rates of denitrification of undisturbed sediment from six lakes as a function of nitrate concentration, oxygen and temperature. Archiv fur Hydrobiologie 80,147-159. Benndorf, J., Uhhnann, D., Piitz, K., 1981. Strategies for water quality management in reservoirs in the German Democratic republic. Water Quality Bulletin 6,68-73. Berge, D., Fjeld, E., Hindar, A., Kaste, O., 1997. Nitrogen retention in two Norwegian watercourses of different trophic status. Ambio 26, 282-288. Bjork, S., 1972. Swedish lake restoration program gets results. Ambio 1, 153-165. Boers, P.C.M., 1996. Nutrient emissions from agriculture in The Netherlands, causes and remedies. Water Science and Technology 33, 183-189.
D.T. van der Molen et al. I Environmental Pollution 102, Sl (1998) 553-557
Caffrey, J.M., Kemp, M., 1992. Influence of the submersed plant, Potamogetonperfoliatus, on nitrogen cycling in estuarine sediments. Limnology and Oceanography 37,1483-1495. Carpenter, S.R., Lodge, D.M., 1986. Effects of submersed macrophytes on ecosystem processes. Aquatic Botany 26,341-370. Codispoti, L.A., 1989. Phosphorus vs. Nitrogen limitation of new and export production. In: W.H. Berger, V.S. Smetacek and G. Wefer (Eds.), Productivity of the Oceans, Present and Past. Wiley, New York, pp. 377-394. Coops, H., Doef, R.W., 1996. Submerged vegetation development in two shallow, eutrophic lakes. Hydrobiologia 340,115-120. De Nobel, W.T., 1998. Ecophysiology of the nitrogen-fixing cyanobacteria Anabaena and Aphanizomenon in relation to eutrophication. Ph.D. thesis, University of Amsterdam, The Netherlands. 99 PP. De Nobel, W.T., Snoep, J.L., Westerhoff, H.V., Mur, L.R., 1997. Interaction of nitrogen furation and phosphorus limitation in Aphanizomenon flos-aquae (Cyanophyceae). Journal of Phycology 33, 794-799. Forsberg, C., Ryding, S.-O., 1985. Research on recovery of polluted lakes. Hur tillfrisknade sjoarna? Vatten 41,3-19 (in Swedish). Foy, R.H., 1986. Suppression of phosphorus release from lake sediments by the addition of nitrate. Water Research 20,1345-1351. Hosper, S.H. (1984) Restoration of Lake Veluwe, The Netherlands, by reduction of phosphorus loading and flushing. Water Science and Technology 17,757-768. Howarth, R.W., Marino, R., Lane, J., Cole, J.J., 1988. Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance. Limnology and Oceanography 33,669-687. Jeppesen, E., Kristensen, P., Jensen, J.P., Sondergaard, M., Mortensen, E., Lauridsen, T., 1991. Recovery resilience following a reduction in external phosphorus loading of shallow, eutrophic Danish lakes: duration, regulating factors and methods for overcoming resilience. Memorie dell’Istituto Italiano di Idrobiologia 48, 127-148. Lauridsen, T.L., Lodge, D.M., 1996. Avoidance by Daphnia magna of fish and macrophytes: chemical cues and predator mediated use of macrophyte habitat. Limnology and Oceanography 41,794-798. Middelburg, J.J., Soetaert, K., Herman, P.M.J., 1996. Evaluation of the nitrogen isotope-pairing method for measuring benthic denitrification: a simulation analysis. Limnology and Oceanography 41, 1839-1844. Ministerie van Verkeer en Waterstaat, 1981. Indicative Water Program 1980-1984. Indicatief Meerjarenprogramma Water 1980-1984. Staatsuitgeverij, ‘s-Gravenhage, ISBN 9012032717 (in Dutch). Ministerie van Verkeer en Waterstaat, 1994. Water in The Netherlands: a time for action. (Water voor Nu en Later.) Voortgangsrapportage Integraal Waterbeheer en Noordzee-aangelegenheden 1994 (in Dutch). Ministerie van Verkeer en Waterstaat, 1997. The Fourth National Policy Document on Watermanagement. Vierde Nota waterhuishouding. Regeringsvoomemen. ISBN 9039913560 (in Dutch). Paerl, H.W., 1990. Physiological ecology and regulation of N, fixation in natural waters. Advances in Microbial Ecology 11,305-344. Peeters, J.C.H., Peperzak, L., 1990. Nutrient limitation in the North Sea: a bioassay approach. Netherlands Journal of Sea Research 26, 61-73. Portielje, R., van der Molen, D.T., 1998a. Relationships between eutrophication variables and system properties in Dutch freshwater lakes. Relaties tussen eutrofilringsvariabelen en systeem-
557
kenmerken van de Nederlandse meren en plassen. Deelrapport II voor de Vierde Eutrofieringsenquete. RIZA rapport 98.007, Lelystad. ISBN 9036951585 (in Dutch). Portielje, R., van der Molen, D.T., 1998b. Trend-analysis of eutrophication variables in lakes in The Netherlands. Water Science and Technology 37,235-240. Ripl, W., 1976. Biochemical oxidation of polluted lake sediment with nitrate -a new lake restoration method. Ambio 5, 132-135. Rysgaard-Petersen, N., Jensen, K., 1997. Nitrification and denitrification in the rhizosphere of the aquatic macrophyte Lobelia dortmanna L. Limnology and Oceanography 42,529-537. Sas, H., 1989. Lake Restoration by Reduction of Nutrient Loading: Expectations, Experiences, Extrapolations. Academia Verlag Richarz GmbH, St. Augustin. ISBN 388345379 X. 497 pp. Schriver, P., Bogestrand, J., Jeppesen, E., Sondergaard, M., 1995. Imact of submerged macrophytes on fish-zooplankton-phytoplankton interactions: large-scale enclosure experiments in a shallow eutrophic lake. Freshwater Biology 33,255-270. Seitzinger, S.P., Nielsen, L.P., Caffrey, J., Christensen, P.B., 1993. Denitrification measurements in aquatic sediments: a comparison of three methods. Biochemistry 23,147-167. Slomp, C.P., van der Gaast, S.J., and van Raaphorst, W., 1996. Phosphorus binding by poorly cristalline iron oxides in North Sea sediments. Marine Chemistry 52,55-73. Sommer, U., 1989. Nutrient status and nutrient competition of phytoplankton in a shallow, hypertrophic lake. Limnology and Oceanography 34,1162-1173. Van Cappellen, P., Ingall, E.D., 1996. Redox stabilization of the atmosphere and oceans by phosphorus-limited marine productivity. Science 27l493-496. Van der Molen, D.T., Boers, P.C.M., 1994. Influence of internal loading on phosphorus concentration in shallow lakes before and after reduction of the external loading. Hydrobiologia 275/276,379-389. Van der Molen, D.T., Boers, P.C.M., Breeuwsma, A., 1998. Agricultural nutrient losses to surface waters in the Netherlands: impact, strategies and perspectives. Journal of Environmental Quality 27, 4-11. Van der Molen, D.T., Los, F.J., van Ballegooijen L., van der Vat, M.P., 1994. Mathematical modelling as a tool for management in eutrophication control of shallow lakes. Hydrobiologia 275/276,479-492. Van Luijn, F., Boers, P.C.M., LijkIema, L., 1996. Comparison of denitrification rates obtained by the N, flux method, the 15N isotope pairing technique and the mass balance approach. Water Research 30,893~900. Van Luijn, F., Boers, P.C.M., LijkIema, L., Sweerts, J.-P.R.A., 1998. Nitrogen fluxes and processes in sandy and muddy sediments from a shallow eutrophic lake. Water Research, in press. Vollenweider, R.A., 1969. Moglichkeiten und Grenzen elementarer Modelle der Stoftbilanz von Seen. Archiv fiir Hydrobiologie 66, l-36 (in German). Wium-Andersen, S., Anthoni, U., Christophersen, C., Houen, G., 1982. Allelopathic effects on phytoplankton by substances isolated from aquatic macrophytes (Charales). Oikos 39, 187-190. Zevenboom, W., 1994. Assessment of eutrophication and its effects in marine waters. German Journal of Hydrography, Supplement 1, 141-170. Zevenboom, W. and Mur, L.R., 1980. N,-fixing cyanobacteria: why they do not become dominant in Dutch, hypertrophic lakes. Developments in Hydrobiology 2,123-130.