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Biological production and eutrophication of Baltic Sea estuarine ecosystems: The Curonian and Vistula Lagoons
Marine Pollution Bulletin 61 (2010) 205–210
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Biological production and eutrophication of Baltic Sea estuarine ecosystems: The Curonian and Vistula Lagoons S.V. Aleksandrov Atlantic Research Institute of Marine Fisheries and Oceanography (AtlantNIRO), 5, Dm. Donskoy Str., Kaliningrad 236000, Russia
a r t i c l e
i n f o
Keywords: Eutrophication Climate change Hyperbloom of Cyanobacteria Curonian and Vistula Lagoons
a b s t r a c t The long-term data on the temporal and spatial changes of chlorophyll and nutrients concentrations, phytoplankton biomass, primary production and mineralization of organic matter in the Curonian and Vistula Lagoons were analyzed using seasonal data to 1994 and monthly data to 2007 at 9–12 stations. A comparison with hydrological (water temperature, salinity, water exchange) and chemical parameters indicate the main abiotic factors which influence the level of biological production and the trophic state of lagoons. Most of the Curonian Lagoon showed the strong summer warming-up of water (higher 20 °C) combined with freshwater conditions, slow-flow velocity and high concentrations of phosphorus which creates conditions for hyperblooms of Cyanobacteria. The biological production of the Vistula Lagoon is below the potentially possible level as the hydrodynamic activity (high-flow velocity) and brackish water prevent the intensive development of Cyanobacteria. The Curonian Lagoon may be considered as hypertrophic water body whereas the Vistula Lagoon is a eutrophic water body. Ó 2010 Published by Elsevier Ltd.
1. Introduction The problems of contamination of coastal and offshore environments and, consequently, of aquatic organisms by pathogenic bacteria and in uncontrolled run-off from urban and agricultural areas, are manifest in the Baltic Sea region (HELCOM, 2002). Eutrophication from the same sources encourages harmful algal blooms that may contaminate fish and shellfish. Coastal lagoons are most vulnerable to direct impacts of natural environmental and anthropogenic factors. Due to this sensitivity, the analysis of long-term changes of chemical and biological parameters in lagoons could demonstrate the actual relationship between global and local changes, including the discrimination of what is ‘‘natural” from what is due to the human action. The Curonian and Vistula Lagoon are the largest coastal lagoons of the Baltic Sea separated from the sea by narrow sand spits. These Lagoons are similar in ground types, mean depths, wind and temperature regimes, however quite different in continental runoff and water salinity. The main morphometric and hydrological characteristics are presented in Table 1. The Curonian and Vistula Lagoons play an important part in many fields of the economies of Russia (Kaliningrad region), Lithuania and Poland. During recent decades, significant anthropogenic changes have occurred in the Lagoons and their watersheds. Ongoing eutrophication is one of the most important problems. Until the late 1980s nutrients loading exceeded by many times the permissible nutrients loading E-mail address: [email protected] 0025-326X/$ - see front matter Ó 2010 Published by Elsevier Ltd. doi:10.1016/j.marpolbul.2010.02.015
leading to eutrophication of water body with such mean depths. Multiple reductions of nutrient loading from the watershed area in 1990s owing to the economic crisis in industry and agriculture did not produce a considerable improvement of the ecological situation. As compared to 1989–1990, the concentration of total nitrogen and phosphorus in the water of the Curonian Lagoon in summer even increased, causing eutrophication. Eutrophication of the Curonian Lagoon affects all trophic levels especially the intensity of phytoplankton development. The research of phytoplankton in the 1980s–2000s showed that the biomass of Cyanobacteria in summer was always at the level of intensive bloom (above 10 g/m3) and during 10 seasons it reached the hyperbloom state (above 100 g/m3) (Aleksandrov and Dmitrieva, 2006; Olenina, 1998; Olenina and Olenin, 2002). This article aims to analyze temporal and spatial changes of biomass and production of phytoplankton, chlorophyll and nutrients concentrations in the water and to evaluate the impact of abiotic factors on biological productivity and ecological conditions of the Lagoons. 2. Material and methods The research was carried out seasonally (from 1993 to 1994) and monthly (from 1995 to 2007) from March to November at 12 standard stations in the Curonian Lagoon and at 9 stations in the Vistula Lagoon (Fig. 1). The hydrological and hydrochemical parameters (water temperature, transparency and salinity, concentration of nutrients, including phosphate, nitrate, ammonia nitrogen, total
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Table 1 Main morphometric and hydrological characteristics of the Curonian and Vistula Lagoons. Description
Unit
Vistula Lagoon
Curonian Lagoon
Total area Volume of water Mean depth Watershed area Continental runoff Inflow from the sea Discharge into the sea Water exchange rate Salinity Secchi depth
km2 km3 m km2 km3/year km3/year km3/year year 1 ‰ m
838 2.3 2.7 23,870 3.6 17.0 20.5 8.9 2.1–5.2 0.45–1.10
1584 6.2 3.8 100,485 20.8 5.1 26.2 4.2 0.1 0.20–0.95
phosphorus and nitrogen) were assessed in water samples from the surface layer with standard methods (ICES, 2004; Koroleff, 1972; Valderrama, 1981). Concentration of chlorophyll a (Chl) was estimated at the surface, at the lower boundary of the photic zone and near the bottom. The concentration Chl a was determined by fluorescent method after 90% acetone extraction of the 0.45 lm filters (Edler, 1979; ICES, 2001). The photosynthesis intensity was measured applying the oxygen modification of the bottle method with short-period (3–5 h) exposition of samples. In calculations of the primary production per unit area (m2) the rates of photosynthesis and mineralization of organic matter were measured at four depth levels of the photic zone (100%, 46%, 10%, 1% of subsurface light intensity), and in the near-bottom layer. The sampling depths of subsurface light intensity were determined with underwater photometer or using the relationship between subsurface light intensity and transparency of water on Secchi disk (O’Relly and Thomas, 1979). The lower boundary of the photic zone was assumed at the depths of 1% of subsurface light intensity (Vollenweider et al., 1974). Generally, but not always, 2.7 time the Secchi depth is close to the 1% light depth in the Curonian and Vistula Lagoons, as well as in many sea and oceanic areas. For consideration of long-term changes of phytoplankton in the Curonian Lagoon the literature data for the period with 1981 for 1996 are used where the intensity of the alga blooms is evaluated
according to the Reimers scale: ‘‘weak” bloom (0.5–0.9 g/m3), ‘‘medium” bloom (1–9.9 g/m3), ‘‘intensive” bloom (10–99 g/m3), ‘‘hyperbloom” (>100 g/m3) (Reimers, 1990; Olenina, 1998). The assessment of water eutrophication of the Curonian and Vistula Lagoons using long-term hydrochemical and hydrobiological data for the period with 1993 for 2007 and carried out according to a trophic classification (Hakanson and Boulion, 2002; Nurnberg, 1996). These classifications (on the basis of Chl a, nutrients and primary production) give four types of trophic state: oligotrophic, mesotrophic, eutrophic and hypertrophic. 3. Results and discussion In the current period, the Curonian Lagoon may be characterized as a highly eutrophic water body on the basis of chemical and biological parameters. The species typically abundant in eutrophic waters prevailed in the phytoplankton (Aphanizomenon flosaquae, Microcystis aeruginosa, Aulacosira islandica, Actinocyclus normanii, Stephanodiscus hantzchii, Stephanodiscus minutulis, etc.) (Aleksandrov and Dmitrieva, 2006). In July–October an intensive development of Cyanobacteria leading to the water ‘‘blooming” was observed in the Curonian Lagoon. The intensive development of Cyanobacteria was recorded during the entire 70-year period of phytoplankton research in the Lagoon. However, in recent decades the phytoplankton biomass increased more than by the order of magnitude – from 34 g/m3 in 1930s and 12 g/m3 in the 1950s to 120–240 g/m3 in the mid-1990s (Olenina, 1998). The research of phytoplankton in the 1980s–2000s showed that biomass of Cyanobacteria in summer was always at the level of intensive bloom (10– 100 g/m3) and during 10 seasons it reached the hyperbloom state (above 100 g/m3) according to the Reimers scale (Reimers, 1990; Olenina, 1998). It is important to note that during three seasons the hyperbloom was observed in the period of the most intensive fertilizers usage in agriculture, while during the remaining blooms occurred during seven seasons in the post-Soviet period when the input of nutrients from the lagoon’s watershed areas decreased considerably (Aleksandrov and Dmitrieva, 2006; Olenina, 1998; Olenina and Olenin, 2002).
Fig. 1. Location of the lagoons in the Baltic Sea (A) and maps of sampling sites in the Curonian (B) and Vistula (C) Lagoons.
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The occurrence of Cyanobacterial blooms resulted from intensive nutrients loading of the Lagoon which occurred up to 1991. During 1989–1990, in the period of maximum fertilizers usage in agriculture and industrial development, the annual input of phosphorus were 3.7–8.5 g/m2 and that of nitrogen – 60.8–109.6 g/m2. The reduction of industrial production and fertilizer usage in the 1990s resulted in a decrease of the external nutrients loading by 3–4 times to 0.75–2.3 g/m2 of phosphorus and to 20.8–40.4 g/m2 of nitrogen per year (Cetkauskaite et al., 2000). As a result it was expected that we would observe a reduction in nutrients concentration in the water and decrease of phytoplankton biomass since the 1990s. However, the research showed that neither a decrease of the trophic status nor an improvement of the ecological situation occurred in the Curonian Lagoon. As compared to the period 1989–1990s, the same high concentration of the total phosphorus and nitrogen are observed, which exceeded the level causing eutrophication of water bodies with such mean depths as those here. The eutrophication processes and water ‘‘blooming” were most pronounced in the southern and central parts (the Russian zone) of the Curonian Lagoon (75% of the area), where the environmental conditions (high concentrations of nutrients in the bed silt, continuously resuspension into the water column due to shallow depths of the Lagoon, absence of the sea water intrusion, slow water ex-
Table 2 Pearson correlation coefficients between average for the growing season (April– October) values water temperature and parameters determining trophic status of water bodies for the period 1993–2007. Index
Curonian Lagoon
Vistula Lagoon
Chlorophyll a Total phosphorus Total nitrogen
0.67 0.72 0.70
0.09 0.29 0.02
A 700
-1
22 20 18 16 14 12 10 8 6 4 2 0
t (°C)
Chl (µg L )
600 500 400 300 200 100 0 IV
V 1
VI
VII VIII IX 2
3
X
change, fresh water) were favouring Cyanobacterial development. Of the hydrological and hydrochemical conditions existing in most parts of the Curonian Lagoon, water temperature appears to be the key factor determining the seasonal and long-tern variability of the primary production and abundance of phytoplankton, and therefore, the level of biological production and the trophic status of the Curonian Lagoon (Table 2). A. flos-aquae, the typical species of highly eutrophicated water bodies, which produces water ‘‘blooming” in the Curonian Lagoon, may develop in the wide range of the water temperatures, however, the optimal temperature causing the reproduction ‘‘outburst”, is observed at water temperature increasing up to 20– 22 °C and more (Whitton, 1973). The temperature optimum of nitrogen fixing for these algae is above 20 °C (Waughman, 1977). Consequently, the abundance of A. flos-aquae permanently present in the Curonian Lagoon during the year increases rapidly (by 100– 1000 times), when the water temperature exceeds 20 °C during several weeks and the weather is warm and calm (Aleksandrov and Dmitrieva, 2006; Olenina, 1998). It is important to note that in the Curonian Lagoon the water temperature exceeds 20 °C only in some ‘‘warm” years. Therefore, in these ‘‘warm” years A. flosaquae formed a high biomass in summer and autumn owing to an ‘‘outburst” reproduction pattern in combination with the consumption of ammonia nitrogen and nitrogen fixation and high concentration of phosphorus in the water, which results in ‘‘hyperblooms” in the Curonian Lagoon. In the years when water temperature does not reach 20 °C, ‘‘hyperblooming” of the Curonian Lagoon is not observed (Fig. 2). As a consequence, the Curonian Lagoon is characterized with high variability of concentration of Chl a, total nitrogen, total phosphorus and others trophic status indices in different years (Fig. 3–5). The mean concentration of total phosphorus for the growing season in 1990s– 2000s varied between 87 and 255 lg P/l, total nitrogen varied between 948 and 3148 lg N/l, Chl a varied between 45 and 186 lg/l,
B 16
-3
-1
VI
VII
t (°C)
PP (gC·m ·day )
14 12 10
22 20 18 16 14 12 10 8 6 4 2 0
8 6 4 2 0
XI Month 4
IV
V
1
VIII
2
IX
X
3
XI Month
4
190 170
15.5 15.0
150 130
14.5
110 14.0
90 70
13.5
Temperature (°C)
Chlorophyll , (µg/l)
Fig. 2. The temperature of water and (A) concentration of chlorophyll a, (B) total primary production in the Curonian Lagoon in 2002 (1, 3) and 2003 (2, 4).
50 30
13.0 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 1
2
Fig. 3. The mean for the growing season (April–October) chlorophyll concentration (1) and temperature of water (2) in the Curonian Lagoon.
3200
15.5
2800
15.0
2400
14.5
2000 14.0
1600
13.5
1200 800
Temperature (°C)
S.V. Aleksandrov / Marine Pollution Bulletin 61 (2010) 205–210
Nitrogen (µg N/l)
208
13.0 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 1
2
260
15.5
230
15.0
200
14.5
170 14.0
140
13.5
110 80
Temperature (°C)
Phosphorus ( µg P/l)
Fig. 4. The mean for the growing season (April–October) total nitrogen (1) and temperature of water (2) in the Curonian Lagoon.
13.0 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 1
2
Fig. 5. The mean for the growing season (April–October) total phosphorus (1) and temperature of water (2) in the Curonian Lagoon.
and total primary production varied between 360 and 620 gC/ (m2year). The estimates obtained to characterize the Curonian Lagoon as a hypertrophic water body for most years of observations (Hakanson and Boulion, 2002; Nurnberg, 1996). The more intensive water warming and the increase in the number of ‘‘warm” years in 1990s–2000s created exceptionally favorable conditions for the development of Cyanobacteria and high rates of primary production. The increase in the number of warm years due to the local climate warming in the Baltic region is a probable reason of the ongoing eutrophication of the Curonian Lagoon despite a significant reduction of external nutrients loading due to the decrease of applying fertilizers and industrial production. In the years of ‘‘hyperblooming” of the Curonian Lagoon, the phytoplankton biomass during the months July–October exceeded the level at which the secondary eutrophication of the water body is observed. On average for the seven years’ period (2001–2007), phytoplankton primary production exceeded mineralization of organic matter by 50% in the Curonian Lagoon. Such a ratio testifies to the accumulation of organic matter in the Lagoon. It produces further eutrophication of the Curonian Lagoon where in the greater part of the water area a slow water exchange is observed. In the Lagoon the concentration of ammonia nitrogen may attain 800– 1000 lg N/l, BOD5 – 10–19 mg O2/l, and pH of water – 9.8–10.0, i.e. the maximum permissible concentrations for fishing water bodies have been considerably exceeded. In the coastal zone, a concentration and decomposition of Cyanobacteria leads to the oxygen deficit through hypoxia to anoxia (16–0% saturation), hydrogen sulphide formation and the death of young fish. These phenomena are of a local nature and determined by the direction of the wind during the ‘‘bloom” period. The years with persistent east winds in July–August resulted in the wind-driven aggregation of Cyanobacteria near the western coast of the Lagoon, which is the most inhabited and recreationally developed area, and thus created the most unfavorable conditions. The resort city of Zelenogradsk and
the National Park of the Curonian Spit are located near western coast of the Curonian Lagoon. Therefore, the warming of the water resulting from global climatic changes represents a risk for coastal water bodies, as this stimulates ‘‘hyperblooms” of Cyanobacteria (for example, A. flos-aquae, M. aeruginosa). The Vistula Lagoon is characterized by a rather low variability of concentrations of Chl a, total nitrogen, total phosphorus and others trophic status indices (Figs. 6–8). The average concentration of total phosphorus for the growing season in the 1990s–2000s varied between 109 and 142 lg P/l, total nitrogen varied between 937 and 1286 lg N/l, Chl a varied between 30 and 48 lg/l and total primary production varied between 316 and 351 g C/(m2 year). Based on several criteria it is possible to conclude that unlike the Curonian Lagoon, eutrophication of the Vistula Lagoon has not attained a critical level. The available estimates of Chl and production allow the Vistula Lagoon to be characterized as a eutrophic water body (Hakanson and Boulion, 2002; Nurnberg, 1996). The values of the primary production, phytoplankton biomass, Chl and nutrients concentrations are considerably lower than in the Curonian Lagoon. Seasonal fluctuations of the hydrochemical indicators of the Lagoon state (BOD5, pH and others) usually do not exceed maximum permissible concentrations for fishing water bodies and consequently no oxygen depletion and death of fish have been observed. The Vistula Lagoon is characterized by a discrepancy between concentrations of Chl a, used as the basis for classifying the water body as eutrophic (from 10 to 100 mg/m3), and total phosphorus concentration typical to hypertrophic water bodies (above 100 lg P/l) (Hakanson and Boulion, 2002). It is assumed that the Chl a concentration reflects the trophic level of the water body, while the total phosphorus content characterizes nutrient loading of the water body and its potential ability to attain a certain level of biological productivity. The biological productivity of the Vistula Lagoon does not attain its potentially possible level. The water exchange between the Lagoon and the Baltic Sea is very important for the water
209
60
17,0
50
16,5 16,0
40
15,5 30
15,0
20
14,5
10
Temperature (°C)
Chlorophyll а, (µg/l)
S.V. Aleksandrov / Marine Pollution Bulletin 61 (2010) 205–210
14,0
0
13,5 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 1
2
1600
17.0
1400
16.5
1200
16.0
1000
15.5
800
15.0
600 400
14.5
200
14.0
0
Temperature (°C)
Nitrogen (µg N/l)
Fig. 6. The mean for the growing season (April–October) chlorophyll concentration (1) and temperature of water (2) in the Vistula Lagoon.
13.5 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 1
2
300
17,0
250
16,5 16,0
200
15,5
150
15,0
100
14,5
50
Temperature (°C)
Phosphorus ( µg P/l)
Fig. 7. The mean for the growing season (April–October) total nitrogen (1) and temperature of water (2) in the Vistula Lagoon.
14,0
0
13,5 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 1
2
Fig. 8. The mean for the growing season (April–October) total phosphorus (1) and temperature of water (2) in the Vistula Lagoon.
body trophic level decrease, since it facilitates the reduction of nutrient concentrations and removes poorly oxidized substances. Hydrodynamic activity (high flowing velocity) and brackish water due to an intensive inflow from the sea prevent the prolonged intensive development of Cyanobacteria, in particular, no ‘‘bloom” A. flos-aquae and M. aeruginosa, causing ‘‘hyperblooming” of the freshwater Curonian Lagoon. The reduction of phytoplankton biomass and primary production with the water salinity increase has been observed in many brackish water bodies of various types. In the Vistula Lagoon the highest concentrations of nutrients and Chl, biomass and production of phytoplankton occurred in the freshwater eastern Russian (Kaliningrad Bay) and southern Polish (Elblong Bay) areas and decreased towards the sea strait in the central part of the Lagoon (Renk et al., 2001). In these hydrological and hydrochemical conditions the water temperature in the Vistula La-
goon is not a key factor determining ‘‘blooming” Cyanobacteria and seasonal and long-term variability of the concentrations of Chl a and nutrients, primary production and therefore, the trophic status of the Vistula Lagoon (Table 2). As a consequence, the local climate warming and more intensive summer warming-up of the water in 1990s–2000s did not significantly affect the biological productivity and ecological state of the brackish Vistula Lagoon, unlike the freshwater Curonian Lagoon.
4. Conclusions On the basis of comparisons with hydrological (water temperature, salinity, hydrodynamic activity) and chemical (nutrients concentration) parameters, the main abiotic factors which influence
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the level of biological production and the trophic state of lagoons can be identified. The strong summer warming of water of the Curonian Lagoon (higher than 20 °C) combined with freshwater conditions, slow-flow velocity and high concentrations of phosphorus creates conditions for hyperblooms of Cyanobacteria ( A. flos-aquae, M. aeruginosa). In the coastal zone the periodical accumulation and decomposition of algae result in an oxygen deficit (reaching anoxic conditions), hydrogen sulphide formation and the death of young fish. In contrast, the biological productivity and trophic state of the Vistula Lagoon do not attain the potentially possible level. Hydrodynamic activity (high flowing velocity) and brackish water prevent the intensive development of Cyanobacteria, in particular, no ‘‘bloom” of A. flos-aquae, M. aeruginosa occurred. The lowest values of primary production, chlorophyll and nutrients concentrations occurred near the Baltic Strait. According to the trophic classification, the Curonian Lagoon may be considered as hypertrophic water body, whereas the Vistula Lagoon is a eutrophic water body. References Aleksandrov, S.V., Dmitrieva, O.A., 2006. Primary production and phytoplankton characteristics as eutrophication criteria of Kursiu Marios Lagoon, the Baltic Sea. Water Resources 33 (1), 97–103. Cetkauskaite, A., Zarkov, D., Stoskus, L., 2000. Water-quality control, monitoring and wastewater treatment in Lithuania 1950 to 1999. Ambio 30 (4–5), 297–305. Edler, L., 1979. Recommendations on methods for marine biological studies in the Baltic Sea. Phytoplankton and chlorophyll. Baltic Marine Biologist 38. Hakanson, L., Boulion, V.V., 2002. The Like Foodweb-Modeling Predation and Abiotic/Biotic Interactions. Backhuys Published, Leiden, 2002, p. 344.
HELCOM, 2002. Environment of the Baltic Sea Area 1994–1998. Baltic Sea Environment Proceedings, vol. 82. p. 216. ICES techniques in marine environmental sciences, 2001. Chlorophyll a: Determination by Spectroscopic Methods, 30. Copenhagen, p. 18. ICES techniques in marine environmental sciences, 2004. Chemical Measurements in the Baltic Sea: Guidelines on Quality Assurance, 35. Copenhagen, p. 149. Koroleff, F., 1972. Determination of dissolved inorganic phosphorus and total phosphorus. Method for sampling and analysis of physical, chemical and biological parameters. Cooperative research report ICES, Series A, vol. 29. pp. 44–49. Nurnberg, G.K., 1996. Trophic state of clear and colored, soft- and hardwaterlakes with special consideration of nutrients, anoxia, phytoplankton and fish. Journal of Lake and Reservoir Management 12, 432–447. Olenina, I., 1998. Long-term changes in the Kursiu Marios lagoon: eutrophication and phytoplankton response. Ecologija 1, 56–65. Olenina, I., Olenin, S., 2002. Environmental problems of the south-eastern Baltic Coast and Curonian Lagoon. Baltic coastal ecosystems. Structure, Function and Coastal Zone Management, 149–156. O’Relly, J., Thomas, J., 1979. A manual for the measurement of total daily primary productivity on marmap and ocean pulse cruises using 14C simulated in situ sunlight incubation. Ocean pulse technical manual, vol. 1. Report No. SHL 79-06. p. 104. Reimers, N.F., 1990. Nature Management. Glossary. Moscow, 1990 (in Russia). Renk, H., Ochock, S., Zalewski, M., 2001. Environmental factors controlling primary production in the Polish part the Vistula Lagoon. Bulletin of Sea Fisheries Institute 1 (152), 78–95. Valderrama, J.C., 1981. The simultaneous analysis of total nitrogen and total phosphorus in natural water. Marine Chemistry 10, 109–122. Vollenweider, R.A., Talling, J.F., Westlake, D.F., 1974. A Manual on Methods for Measuring Primary Production in Aquatic Environments. Backwell Scientific Publications, p. 214. Waughman, G.J., 1977. The effect of temperature on nitrogenase activity. Journal of Experimental Botany 28 (105), 949–960. Whitton, B.A., 1973. Freshwater plankton. The Biology of Blue-Green Algae 9, 353– 367.
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Biological production and eutrophication of Baltic Sea estuarine ecosystems: The Curonian and Vistula Lagoons S.V. Aleksandrov Atlantic Research Institute of Marine Fisheries and Oceanography (AtlantNIRO), 5, Dm. Donskoy Str., Kaliningrad 236000, Russia
a r t i c l e
i n f o
Keywords: Eutrophication Climate change Hyperbloom of Cyanobacteria Curonian and Vistula Lagoons
a b s t r a c t The long-term data on the temporal and spatial changes of chlorophyll and nutrients concentrations, phytoplankton biomass, primary production and mineralization of organic matter in the Curonian and Vistula Lagoons were analyzed using seasonal data to 1994 and monthly data to 2007 at 9–12 stations. A comparison with hydrological (water temperature, salinity, water exchange) and chemical parameters indicate the main abiotic factors which influence the level of biological production and the trophic state of lagoons. Most of the Curonian Lagoon showed the strong summer warming-up of water (higher 20 °C) combined with freshwater conditions, slow-flow velocity and high concentrations of phosphorus which creates conditions for hyperblooms of Cyanobacteria. The biological production of the Vistula Lagoon is below the potentially possible level as the hydrodynamic activity (high-flow velocity) and brackish water prevent the intensive development of Cyanobacteria. The Curonian Lagoon may be considered as hypertrophic water body whereas the Vistula Lagoon is a eutrophic water body. Ó 2010 Published by Elsevier Ltd.
1. Introduction The problems of contamination of coastal and offshore environments and, consequently, of aquatic organisms by pathogenic bacteria and in uncontrolled run-off from urban and agricultural areas, are manifest in the Baltic Sea region (HELCOM, 2002). Eutrophication from the same sources encourages harmful algal blooms that may contaminate fish and shellfish. Coastal lagoons are most vulnerable to direct impacts of natural environmental and anthropogenic factors. Due to this sensitivity, the analysis of long-term changes of chemical and biological parameters in lagoons could demonstrate the actual relationship between global and local changes, including the discrimination of what is ‘‘natural” from what is due to the human action. The Curonian and Vistula Lagoon are the largest coastal lagoons of the Baltic Sea separated from the sea by narrow sand spits. These Lagoons are similar in ground types, mean depths, wind and temperature regimes, however quite different in continental runoff and water salinity. The main morphometric and hydrological characteristics are presented in Table 1. The Curonian and Vistula Lagoons play an important part in many fields of the economies of Russia (Kaliningrad region), Lithuania and Poland. During recent decades, significant anthropogenic changes have occurred in the Lagoons and their watersheds. Ongoing eutrophication is one of the most important problems. Until the late 1980s nutrients loading exceeded by many times the permissible nutrients loading E-mail address: [email protected] 0025-326X/$ - see front matter Ó 2010 Published by Elsevier Ltd. doi:10.1016/j.marpolbul.2010.02.015
leading to eutrophication of water body with such mean depths. Multiple reductions of nutrient loading from the watershed area in 1990s owing to the economic crisis in industry and agriculture did not produce a considerable improvement of the ecological situation. As compared to 1989–1990, the concentration of total nitrogen and phosphorus in the water of the Curonian Lagoon in summer even increased, causing eutrophication. Eutrophication of the Curonian Lagoon affects all trophic levels especially the intensity of phytoplankton development. The research of phytoplankton in the 1980s–2000s showed that the biomass of Cyanobacteria in summer was always at the level of intensive bloom (above 10 g/m3) and during 10 seasons it reached the hyperbloom state (above 100 g/m3) (Aleksandrov and Dmitrieva, 2006; Olenina, 1998; Olenina and Olenin, 2002). This article aims to analyze temporal and spatial changes of biomass and production of phytoplankton, chlorophyll and nutrients concentrations in the water and to evaluate the impact of abiotic factors on biological productivity and ecological conditions of the Lagoons. 2. Material and methods The research was carried out seasonally (from 1993 to 1994) and monthly (from 1995 to 2007) from March to November at 12 standard stations in the Curonian Lagoon and at 9 stations in the Vistula Lagoon (Fig. 1). The hydrological and hydrochemical parameters (water temperature, transparency and salinity, concentration of nutrients, including phosphate, nitrate, ammonia nitrogen, total
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S.V. Aleksandrov / Marine Pollution Bulletin 61 (2010) 205–210
Table 1 Main morphometric and hydrological characteristics of the Curonian and Vistula Lagoons. Description
Unit
Vistula Lagoon
Curonian Lagoon
Total area Volume of water Mean depth Watershed area Continental runoff Inflow from the sea Discharge into the sea Water exchange rate Salinity Secchi depth
km2 km3 m km2 km3/year km3/year km3/year year 1 ‰ m
838 2.3 2.7 23,870 3.6 17.0 20.5 8.9 2.1–5.2 0.45–1.10
1584 6.2 3.8 100,485 20.8 5.1 26.2 4.2 0.1 0.20–0.95
phosphorus and nitrogen) were assessed in water samples from the surface layer with standard methods (ICES, 2004; Koroleff, 1972; Valderrama, 1981). Concentration of chlorophyll a (Chl) was estimated at the surface, at the lower boundary of the photic zone and near the bottom. The concentration Chl a was determined by fluorescent method after 90% acetone extraction of the 0.45 lm filters (Edler, 1979; ICES, 2001). The photosynthesis intensity was measured applying the oxygen modification of the bottle method with short-period (3–5 h) exposition of samples. In calculations of the primary production per unit area (m2) the rates of photosynthesis and mineralization of organic matter were measured at four depth levels of the photic zone (100%, 46%, 10%, 1% of subsurface light intensity), and in the near-bottom layer. The sampling depths of subsurface light intensity were determined with underwater photometer or using the relationship between subsurface light intensity and transparency of water on Secchi disk (O’Relly and Thomas, 1979). The lower boundary of the photic zone was assumed at the depths of 1% of subsurface light intensity (Vollenweider et al., 1974). Generally, but not always, 2.7 time the Secchi depth is close to the 1% light depth in the Curonian and Vistula Lagoons, as well as in many sea and oceanic areas. For consideration of long-term changes of phytoplankton in the Curonian Lagoon the literature data for the period with 1981 for 1996 are used where the intensity of the alga blooms is evaluated
according to the Reimers scale: ‘‘weak” bloom (0.5–0.9 g/m3), ‘‘medium” bloom (1–9.9 g/m3), ‘‘intensive” bloom (10–99 g/m3), ‘‘hyperbloom” (>100 g/m3) (Reimers, 1990; Olenina, 1998). The assessment of water eutrophication of the Curonian and Vistula Lagoons using long-term hydrochemical and hydrobiological data for the period with 1993 for 2007 and carried out according to a trophic classification (Hakanson and Boulion, 2002; Nurnberg, 1996). These classifications (on the basis of Chl a, nutrients and primary production) give four types of trophic state: oligotrophic, mesotrophic, eutrophic and hypertrophic. 3. Results and discussion In the current period, the Curonian Lagoon may be characterized as a highly eutrophic water body on the basis of chemical and biological parameters. The species typically abundant in eutrophic waters prevailed in the phytoplankton (Aphanizomenon flosaquae, Microcystis aeruginosa, Aulacosira islandica, Actinocyclus normanii, Stephanodiscus hantzchii, Stephanodiscus minutulis, etc.) (Aleksandrov and Dmitrieva, 2006). In July–October an intensive development of Cyanobacteria leading to the water ‘‘blooming” was observed in the Curonian Lagoon. The intensive development of Cyanobacteria was recorded during the entire 70-year period of phytoplankton research in the Lagoon. However, in recent decades the phytoplankton biomass increased more than by the order of magnitude – from 34 g/m3 in 1930s and 12 g/m3 in the 1950s to 120–240 g/m3 in the mid-1990s (Olenina, 1998). The research of phytoplankton in the 1980s–2000s showed that biomass of Cyanobacteria in summer was always at the level of intensive bloom (10– 100 g/m3) and during 10 seasons it reached the hyperbloom state (above 100 g/m3) according to the Reimers scale (Reimers, 1990; Olenina, 1998). It is important to note that during three seasons the hyperbloom was observed in the period of the most intensive fertilizers usage in agriculture, while during the remaining blooms occurred during seven seasons in the post-Soviet period when the input of nutrients from the lagoon’s watershed areas decreased considerably (Aleksandrov and Dmitrieva, 2006; Olenina, 1998; Olenina and Olenin, 2002).
Fig. 1. Location of the lagoons in the Baltic Sea (A) and maps of sampling sites in the Curonian (B) and Vistula (C) Lagoons.
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The occurrence of Cyanobacterial blooms resulted from intensive nutrients loading of the Lagoon which occurred up to 1991. During 1989–1990, in the period of maximum fertilizers usage in agriculture and industrial development, the annual input of phosphorus were 3.7–8.5 g/m2 and that of nitrogen – 60.8–109.6 g/m2. The reduction of industrial production and fertilizer usage in the 1990s resulted in a decrease of the external nutrients loading by 3–4 times to 0.75–2.3 g/m2 of phosphorus and to 20.8–40.4 g/m2 of nitrogen per year (Cetkauskaite et al., 2000). As a result it was expected that we would observe a reduction in nutrients concentration in the water and decrease of phytoplankton biomass since the 1990s. However, the research showed that neither a decrease of the trophic status nor an improvement of the ecological situation occurred in the Curonian Lagoon. As compared to the period 1989–1990s, the same high concentration of the total phosphorus and nitrogen are observed, which exceeded the level causing eutrophication of water bodies with such mean depths as those here. The eutrophication processes and water ‘‘blooming” were most pronounced in the southern and central parts (the Russian zone) of the Curonian Lagoon (75% of the area), where the environmental conditions (high concentrations of nutrients in the bed silt, continuously resuspension into the water column due to shallow depths of the Lagoon, absence of the sea water intrusion, slow water ex-
Table 2 Pearson correlation coefficients between average for the growing season (April– October) values water temperature and parameters determining trophic status of water bodies for the period 1993–2007. Index
Curonian Lagoon
Vistula Lagoon
Chlorophyll a Total phosphorus Total nitrogen
0.67 0.72 0.70
0.09 0.29 0.02
A 700
-1
22 20 18 16 14 12 10 8 6 4 2 0
t (°C)
Chl (µg L )
600 500 400 300 200 100 0 IV
V 1
VI
VII VIII IX 2
3
X
change, fresh water) were favouring Cyanobacterial development. Of the hydrological and hydrochemical conditions existing in most parts of the Curonian Lagoon, water temperature appears to be the key factor determining the seasonal and long-tern variability of the primary production and abundance of phytoplankton, and therefore, the level of biological production and the trophic status of the Curonian Lagoon (Table 2). A. flos-aquae, the typical species of highly eutrophicated water bodies, which produces water ‘‘blooming” in the Curonian Lagoon, may develop in the wide range of the water temperatures, however, the optimal temperature causing the reproduction ‘‘outburst”, is observed at water temperature increasing up to 20– 22 °C and more (Whitton, 1973). The temperature optimum of nitrogen fixing for these algae is above 20 °C (Waughman, 1977). Consequently, the abundance of A. flos-aquae permanently present in the Curonian Lagoon during the year increases rapidly (by 100– 1000 times), when the water temperature exceeds 20 °C during several weeks and the weather is warm and calm (Aleksandrov and Dmitrieva, 2006; Olenina, 1998). It is important to note that in the Curonian Lagoon the water temperature exceeds 20 °C only in some ‘‘warm” years. Therefore, in these ‘‘warm” years A. flosaquae formed a high biomass in summer and autumn owing to an ‘‘outburst” reproduction pattern in combination with the consumption of ammonia nitrogen and nitrogen fixation and high concentration of phosphorus in the water, which results in ‘‘hyperblooms” in the Curonian Lagoon. In the years when water temperature does not reach 20 °C, ‘‘hyperblooming” of the Curonian Lagoon is not observed (Fig. 2). As a consequence, the Curonian Lagoon is characterized with high variability of concentration of Chl a, total nitrogen, total phosphorus and others trophic status indices in different years (Fig. 3–5). The mean concentration of total phosphorus for the growing season in 1990s– 2000s varied between 87 and 255 lg P/l, total nitrogen varied between 948 and 3148 lg N/l, Chl a varied between 45 and 186 lg/l,
B 16
-3
-1
VI
VII
t (°C)
PP (gC·m ·day )
14 12 10
22 20 18 16 14 12 10 8 6 4 2 0
8 6 4 2 0
XI Month 4
IV
V
1
VIII
2
IX
X
3
XI Month
4
190 170
15.5 15.0
150 130
14.5
110 14.0
90 70
13.5
Temperature (°C)
Chlorophyll , (µg/l)
Fig. 2. The temperature of water and (A) concentration of chlorophyll a, (B) total primary production in the Curonian Lagoon in 2002 (1, 3) and 2003 (2, 4).
50 30
13.0 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 1
2
Fig. 3. The mean for the growing season (April–October) chlorophyll concentration (1) and temperature of water (2) in the Curonian Lagoon.
3200
15.5
2800
15.0
2400
14.5
2000 14.0
1600
13.5
1200 800
Temperature (°C)
S.V. Aleksandrov / Marine Pollution Bulletin 61 (2010) 205–210
Nitrogen (µg N/l)
208
13.0 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 1
2
260
15.5
230
15.0
200
14.5
170 14.0
140
13.5
110 80
Temperature (°C)
Phosphorus ( µg P/l)
Fig. 4. The mean for the growing season (April–October) total nitrogen (1) and temperature of water (2) in the Curonian Lagoon.
13.0 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 1
2
Fig. 5. The mean for the growing season (April–October) total phosphorus (1) and temperature of water (2) in the Curonian Lagoon.
and total primary production varied between 360 and 620 gC/ (m2year). The estimates obtained to characterize the Curonian Lagoon as a hypertrophic water body for most years of observations (Hakanson and Boulion, 2002; Nurnberg, 1996). The more intensive water warming and the increase in the number of ‘‘warm” years in 1990s–2000s created exceptionally favorable conditions for the development of Cyanobacteria and high rates of primary production. The increase in the number of warm years due to the local climate warming in the Baltic region is a probable reason of the ongoing eutrophication of the Curonian Lagoon despite a significant reduction of external nutrients loading due to the decrease of applying fertilizers and industrial production. In the years of ‘‘hyperblooming” of the Curonian Lagoon, the phytoplankton biomass during the months July–October exceeded the level at which the secondary eutrophication of the water body is observed. On average for the seven years’ period (2001–2007), phytoplankton primary production exceeded mineralization of organic matter by 50% in the Curonian Lagoon. Such a ratio testifies to the accumulation of organic matter in the Lagoon. It produces further eutrophication of the Curonian Lagoon where in the greater part of the water area a slow water exchange is observed. In the Lagoon the concentration of ammonia nitrogen may attain 800– 1000 lg N/l, BOD5 – 10–19 mg O2/l, and pH of water – 9.8–10.0, i.e. the maximum permissible concentrations for fishing water bodies have been considerably exceeded. In the coastal zone, a concentration and decomposition of Cyanobacteria leads to the oxygen deficit through hypoxia to anoxia (16–0% saturation), hydrogen sulphide formation and the death of young fish. These phenomena are of a local nature and determined by the direction of the wind during the ‘‘bloom” period. The years with persistent east winds in July–August resulted in the wind-driven aggregation of Cyanobacteria near the western coast of the Lagoon, which is the most inhabited and recreationally developed area, and thus created the most unfavorable conditions. The resort city of Zelenogradsk and
the National Park of the Curonian Spit are located near western coast of the Curonian Lagoon. Therefore, the warming of the water resulting from global climatic changes represents a risk for coastal water bodies, as this stimulates ‘‘hyperblooms” of Cyanobacteria (for example, A. flos-aquae, M. aeruginosa). The Vistula Lagoon is characterized by a rather low variability of concentrations of Chl a, total nitrogen, total phosphorus and others trophic status indices (Figs. 6–8). The average concentration of total phosphorus for the growing season in the 1990s–2000s varied between 109 and 142 lg P/l, total nitrogen varied between 937 and 1286 lg N/l, Chl a varied between 30 and 48 lg/l and total primary production varied between 316 and 351 g C/(m2 year). Based on several criteria it is possible to conclude that unlike the Curonian Lagoon, eutrophication of the Vistula Lagoon has not attained a critical level. The available estimates of Chl and production allow the Vistula Lagoon to be characterized as a eutrophic water body (Hakanson and Boulion, 2002; Nurnberg, 1996). The values of the primary production, phytoplankton biomass, Chl and nutrients concentrations are considerably lower than in the Curonian Lagoon. Seasonal fluctuations of the hydrochemical indicators of the Lagoon state (BOD5, pH and others) usually do not exceed maximum permissible concentrations for fishing water bodies and consequently no oxygen depletion and death of fish have been observed. The Vistula Lagoon is characterized by a discrepancy between concentrations of Chl a, used as the basis for classifying the water body as eutrophic (from 10 to 100 mg/m3), and total phosphorus concentration typical to hypertrophic water bodies (above 100 lg P/l) (Hakanson and Boulion, 2002). It is assumed that the Chl a concentration reflects the trophic level of the water body, while the total phosphorus content characterizes nutrient loading of the water body and its potential ability to attain a certain level of biological productivity. The biological productivity of the Vistula Lagoon does not attain its potentially possible level. The water exchange between the Lagoon and the Baltic Sea is very important for the water
209
60
17,0
50
16,5 16,0
40
15,5 30
15,0
20
14,5
10
Temperature (°C)
Chlorophyll а, (µg/l)
S.V. Aleksandrov / Marine Pollution Bulletin 61 (2010) 205–210
14,0
0
13,5 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 1
2
1600
17.0
1400
16.5
1200
16.0
1000
15.5
800
15.0
600 400
14.5
200
14.0
0
Temperature (°C)
Nitrogen (µg N/l)
Fig. 6. The mean for the growing season (April–October) chlorophyll concentration (1) and temperature of water (2) in the Vistula Lagoon.
13.5 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 1
2
300
17,0
250
16,5 16,0
200
15,5
150
15,0
100
14,5
50
Temperature (°C)
Phosphorus ( µg P/l)
Fig. 7. The mean for the growing season (April–October) total nitrogen (1) and temperature of water (2) in the Vistula Lagoon.
14,0
0
13,5 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 1
2
Fig. 8. The mean for the growing season (April–October) total phosphorus (1) and temperature of water (2) in the Vistula Lagoon.
body trophic level decrease, since it facilitates the reduction of nutrient concentrations and removes poorly oxidized substances. Hydrodynamic activity (high flowing velocity) and brackish water due to an intensive inflow from the sea prevent the prolonged intensive development of Cyanobacteria, in particular, no ‘‘bloom” A. flos-aquae and M. aeruginosa, causing ‘‘hyperblooming” of the freshwater Curonian Lagoon. The reduction of phytoplankton biomass and primary production with the water salinity increase has been observed in many brackish water bodies of various types. In the Vistula Lagoon the highest concentrations of nutrients and Chl, biomass and production of phytoplankton occurred in the freshwater eastern Russian (Kaliningrad Bay) and southern Polish (Elblong Bay) areas and decreased towards the sea strait in the central part of the Lagoon (Renk et al., 2001). In these hydrological and hydrochemical conditions the water temperature in the Vistula La-
goon is not a key factor determining ‘‘blooming” Cyanobacteria and seasonal and long-term variability of the concentrations of Chl a and nutrients, primary production and therefore, the trophic status of the Vistula Lagoon (Table 2). As a consequence, the local climate warming and more intensive summer warming-up of the water in 1990s–2000s did not significantly affect the biological productivity and ecological state of the brackish Vistula Lagoon, unlike the freshwater Curonian Lagoon.
4. Conclusions On the basis of comparisons with hydrological (water temperature, salinity, hydrodynamic activity) and chemical (nutrients concentration) parameters, the main abiotic factors which influence
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the level of biological production and the trophic state of lagoons can be identified. The strong summer warming of water of the Curonian Lagoon (higher than 20 °C) combined with freshwater conditions, slow-flow velocity and high concentrations of phosphorus creates conditions for hyperblooms of Cyanobacteria ( A. flos-aquae, M. aeruginosa). In the coastal zone the periodical accumulation and decomposition of algae result in an oxygen deficit (reaching anoxic conditions), hydrogen sulphide formation and the death of young fish. In contrast, the biological productivity and trophic state of the Vistula Lagoon do not attain the potentially possible level. Hydrodynamic activity (high flowing velocity) and brackish water prevent the intensive development of Cyanobacteria, in particular, no ‘‘bloom” of A. flos-aquae, M. aeruginosa occurred. The lowest values of primary production, chlorophyll and nutrients concentrations occurred near the Baltic Strait. According to the trophic classification, the Curonian Lagoon may be considered as hypertrophic water body, whereas the Vistula Lagoon is a eutrophic water body. References Aleksandrov, S.V., Dmitrieva, O.A., 2006. Primary production and phytoplankton characteristics as eutrophication criteria of Kursiu Marios Lagoon, the Baltic Sea. Water Resources 33 (1), 97–103. Cetkauskaite, A., Zarkov, D., Stoskus, L., 2000. Water-quality control, monitoring and wastewater treatment in Lithuania 1950 to 1999. Ambio 30 (4–5), 297–305. Edler, L., 1979. Recommendations on methods for marine biological studies in the Baltic Sea. Phytoplankton and chlorophyll. Baltic Marine Biologist 38. Hakanson, L., Boulion, V.V., 2002. The Like Foodweb-Modeling Predation and Abiotic/Biotic Interactions. Backhuys Published, Leiden, 2002, p. 344.
HELCOM, 2002. Environment of the Baltic Sea Area 1994–1998. Baltic Sea Environment Proceedings, vol. 82. p. 216. ICES techniques in marine environmental sciences, 2001. Chlorophyll a: Determination by Spectroscopic Methods, 30. Copenhagen, p. 18. ICES techniques in marine environmental sciences, 2004. Chemical Measurements in the Baltic Sea: Guidelines on Quality Assurance, 35. Copenhagen, p. 149. Koroleff, F., 1972. Determination of dissolved inorganic phosphorus and total phosphorus. Method for sampling and analysis of physical, chemical and biological parameters. Cooperative research report ICES, Series A, vol. 29. pp. 44–49. Nurnberg, G.K., 1996. Trophic state of clear and colored, soft- and hardwaterlakes with special consideration of nutrients, anoxia, phytoplankton and fish. Journal of Lake and Reservoir Management 12, 432–447. Olenina, I., 1998. Long-term changes in the Kursiu Marios lagoon: eutrophication and phytoplankton response. Ecologija 1, 56–65. Olenina, I., Olenin, S., 2002. Environmental problems of the south-eastern Baltic Coast and Curonian Lagoon. Baltic coastal ecosystems. Structure, Function and Coastal Zone Management, 149–156. O’Relly, J., Thomas, J., 1979. A manual for the measurement of total daily primary productivity on marmap and ocean pulse cruises using 14C simulated in situ sunlight incubation. Ocean pulse technical manual, vol. 1. Report No. SHL 79-06. p. 104. Reimers, N.F., 1990. Nature Management. Glossary. Moscow, 1990 (in Russia). Renk, H., Ochock, S., Zalewski, M., 2001. Environmental factors controlling primary production in the Polish part the Vistula Lagoon. Bulletin of Sea Fisheries Institute 1 (152), 78–95. Valderrama, J.C., 1981. The simultaneous analysis of total nitrogen and total phosphorus in natural water. Marine Chemistry 10, 109–122. Vollenweider, R.A., Talling, J.F., Westlake, D.F., 1974. A Manual on Methods for Measuring Primary Production in Aquatic Environments. Backwell Scientific Publications, p. 214. Waughman, G.J., 1977. The effect of temperature on nitrogenase activity. Journal of Experimental Botany 28 (105), 949–960. Whitton, B.A., 1973. Freshwater plankton. The Biology of Blue-Green Algae 9, 353– 367.