Large Lake Peipsi (3555 km2) is divided between two countries, Estonia (44%) and Russia (56%). The southernmost part of the lake, Lake Pihkva, is almost entirely (99%) in Russia, and is continuously being polluted by the greatest inflow to Lake Peipsi, the insufficiently purified River Velikaya. Research on this lake (Lake Peipsi) in the growing season has been possible as a result of Estonian–Russian joint expeditions (2003–2010) in the month of August. Our study has demonstrated statistically significant variances in the hydrochemistry and zoo- and phytoplankton data between the lake parts. Several parameters used for characterizing the lake's ecosystem were considerably higher for Lake Pihkva than for the larger Lake Peipsi s.s. These include increases in TP concentration (3×); TN (2×); Chlorophyll a (3×); biomass of cyanobacteria (4×); Microcystis (4×); Aphanizomenon (5×); abundance of Chydorus sphaericus (5×); Keratella tecta (8×). However, several values were lower in Lake Pihkva than in Lake Peipsi: water transparency (3×); ratio between zoo- and phytoplankton biomasses (2×); cladoceran mean weight (3×); abundance of Eudiaptomus gracilis (1.5×); abundance of Kellicottia longispina (1.8×). Different natural conditions (topography, catchment area, relative depth) and different pollution loads in the lake parts have resulted in apparently different resistances in their ecosystems and different responses to human activity. At present, on the basis of TP data (up to 200 mg m−3), Lake Pihkva appears to act a polluter of adjacent lake part rather than a purification pond.
Lake Peipsi is located on the Estonian-Russian border and is the largest transboundary lake in Europe. It consists of three different basins: the northern, largest part (surface area 2611 km2, mean depth 8.1 m) is the eutrophic Lake Peipsi s.s. (sensu stricto); the southernmost part is the hypertrophic Lake Pihkva (708 km2, 3.8 m), which is connected with Lake Peipsi s.s. by the third part, the river-like Lake Lämmijärv (236 km2, 2.5 m). Of the 3555 km2 total lake surface area, 44% is in Estonia, and 56% in Russia (Figure 1). The drainage basin of the lake is 47,814 km2 of which 58% is located in Russian territory, 34% in Estonia and 8% in Latvia. A main source of lake pollution is two rivers (other rivers are much smaller). The biggest inflow is from the Velikaya River, draining into Lake Pihkva, mostly from Russian territory, with a draining area of 25,500 km2. This covers 53.3% of the total draining basin of the lake. The second largest river is the Emajõgi River, draining into Lake Peipsi s.s., with a draining area of 9,960 km2 (16.1%). The largest point pollution sources for Lake Peipsi are the town of Tartu (100,000 inhabitants), situated on the banks of the River Emajõgi, and the town of Pskov (200,000 inhabitants) on the banks of the River Velikaya. Since 1998 the wastewaters from Tartu have been purified biologically and chemically, and the efficiency of phosphorus removal is approximately 85–90%. Wastewaters from Pskov are purified only biologically, and phosphorus is not yet being removed (Loigu et al., 2008). As Lake Peipsi is divided between two countries, examinations and analyses of Lake Pihkva, belonging almost entirely (98.7%) to Russia, have been possible only as a result of Estonian-Russian joint expeditions (carried out in the month of August between 2003 and 2010). The data obtained for Lake Pihkva has allowed us to make reliable comparisons between the ecosystems of all three lake parts. Nutrient loads from Estonia and Russia have always differed. It has previously been estimated that approximately 63% of the total nitrogen (TN) and 68% of the total phosphorus (TP) were carried into Lake Pihkva via rivers in the Russian territory (Stålnake et al., 2002).
In the mid-1990s, the loading of nutrients into Lake Peipsi from the Estonian lake catchment decreased, whereas P loading from the Russian lake catchment increased (Nõges et al., 2010). Pronounced ecological effects of reduced nutrient loading have been found in many European lakes (Jeppesen et al., 2005; Rask et al., 2011; Arvola et al., 2011). However, it should be noted that the changes in the nutrient supply of lakes in Western European countries has been different from that in countries of the former Soviet Union. In the Western countries, efforts have been made to reduce phosphorus concentration in effluents (Jeppesen et al., 2005). In Estonia and Russia, on the other hand, there was a major reduction in nitrogen (N) as a result of reduced agriculture (Blinova, 2001). In these countries, when adequate purification of point sources did not follow, continuing eutrophication of the lake could be expected.
Since the late 1990s and during the 2000s, the ecosystem of Lake Peipsi lost its stability (Kangur and Möls, 2008; Haberman et al., 2010). Nõges et al. (2005) explained this destabilization of the ecosystem as due to a decrease in the N:P ratio, caused by increased phosphorus and reduced nitrogen loading. The proportion of cyanobacteria in the total biomass of summer phytoplankton increased at a constant rate, from 20% to 70% in Lake Peipsi s.s. and from 30% to 80% in Lake Pihkva. An appreciable concentration of microcystins was detected in the open water regions in summer months (Tanner et al., 2005), and the biomass of the genus Microcystis exceeded 20 g m−3 in some years in the southern lake parts. Several studies have indicated the harmful effects of the toxins and bloom extracts on zooplankton (Gilbert, 1994; Barreiro et al., 2007). In parallel with increasing cyanobacterial blooms, a marked decline has occurred in zooplankton (Haberman et al., 2010), and consequent changes in fish populations. The stock of planktivorous lake smelt (Osmerus eperlanus m. spirinchus Pallas) and vendace (Coregonus albula (L)) have decreased drastically. A heavy fish kill has occurred in the hot summer months in some years (Kangur et al., 2005).
In the present study we have documented the heterogenity of the ecosystems of Lake Peipsi, focusing on peculiarities found in the southernmost tip of the lake, Lake Pihkva. We conjectured that Lake Pihkva might be a calculable polluter for the adjacent lake part.
Materials and Methods
The material for the present study was collected from 15 sampling spots in Lake Peipsi in August from 2003 to 2010. Samples for phyto- and zooplankton analysis were obtained in parallel with those to be used for measurements of hydrochemical data. The material was obtained by mixing each sample of water collected using a 2 litre Van Dorn sampler, at 1 m depth intervals through the entire water column. Water for phytoplankton analysis was taken directly from this vessel, while for zooplankton, 20 litres was filtered through a net with mesh size 48 μm. Both plankton samples were preserved with Lugol's (acidified iodine) solution. The methods used for treating samples and biomass estimation for phyto-and zooplankton were common. Hydrochemical samples were analysed by Tartu Environmental Researchers Ltd., Estonia. Hydrochemical parameters were log-transformed and their average values were expressed as geometric means. Arithmetic means were used for plankton abundances. Estimation of differences between lake parts was carried out with the estimate command of the GENMOD procedure. To describe the trophic state of the lake principal component analysis was used. The first principal component calculated was named as trophy index (TI). This trophic index was compared to Carlson's trophic indices (Carlson, 1977), which revealed high correlations (r 0.96 in case of TSISD, 0.92 by TSIChl, 0.95 by TSITP, p < 0.0001). Spearman correlations were then used to explore relationships between TI and different plankton parameters. Statistical analyses were carried out using the procedures of SAS/STAT version 9.2 (SAS Institute, 2009).
Results and Discussion
Long-term investigations have demonstrated that the water chemistry of the large Lake Peipsi varies from north to south (Kangur and Möls, 2008; Haberman et al., 2010). According to our data for the month of August between 2003 and 2010, significant differences ( p < 0.0001) between the lake parts was revealed (Tables 1 and 2). The highly correlated (R2 > 0.8) water parameters—TP, TN, Chla and transparency—described most of the variability found in the hydrochemical data. The first principal component, trophy index (TI), explained 67% of the variance. The spatial variability found in the first principal component calculated for Lake Peipsi demonstrated clearly the polarity of the lake (Figure 2). Rumyantsev et al. (2005) has stated that 60% of the phosphorus discharged into Lake Pihkva remains in that lake and does not contribute to the eutrophication of Lake Peipsi s.s. Also, Nõges et al. (2005) have stated that the southernmost part of Lake Peipsi acts as a purification pond for Lake Peipsi s.s. As Lake Pihkva is shallow and highly influenced by wind action, any phosphorus discharged into the lake to a large degree cannot be retarded only in sediments. Instead, it moves into the water column and the pollution of the lake is thus great. Different conditions (topography, catchment area, relative depth, external and internal loading) affect the different resistances of any ecosystem (Jeppesen et al., 2005; Kõiv et al., 2011). The resistance of the three different parts of Lake Peipsi do differ. It appears that the ecosystem of Lake Pihkva is losing its resilience (Kangur and Möls, 2008; Haberman et al., 2010), and thus it is difficult to believe in the ability of the lake to function as a strong purification pond. Not denying some of the purification effects of Lake Pihkva, its polluting effects on the neighbouring Lake Lämmijärv are evident (Table 1, Figure 2).
From measurements taken in the month of August from 2003 to 2010, it can be observed that the biomasses of phytoplankton, cyanobacteria, Microcystis and Aphanizomenon, as well as chlorophyll a content in Lake Peipsi clearly differed in the north and south lake parts (Table 1). As a rule, the levels in the south were greater than those in the north. In Lake Pihkva, in the south, the biomass of phytoplankton was on an average three times, and that of cyanobacteria four times higher than in Lake Peipsi s.s. in the north; corresponding data for the cyanobacteria Microcystis spp. and Aphanizomenon flos-aquae Ralfs showed them to be 4× and 5× higher, respectively. Phytoplankton data were quite similar for lakes Lämmijärv and Pihkva, and mostly different from the northern part of the lake, Lake Peipsi s.s. Phytoplankton biomass and chl a, both indicators of eutrophication, have been used successfully in assessing the ecological status of Finnish lakes (Arvola et al., 2011; Rask et al., 2011). According to Downing et al. (2001), cyanobacteria generally represent an average of approximately 60% of the phytoplankton biomass at TP above 80–90 μg l−1. In Lake Peipsi the proportion of cyanobacteria was 58% at mean TP content 46 μg l−1, 65% at 87 μg l−1 and 73% at 121 μg l−1.
The correlation analysis applied to the data in this study has shown definite relationships between several zooplankton indicators and the calculated trophy index, TI (Table 2). The zooplankton-phytoplankton biomass ratio (BZp/BPhyt) in Lake Peipsi s.s. was 2.2 times greater than in Lake Pihkva (Table 1). A decrease in the BZp/BPhyt ratio with an increase in the trophic state of a lake has been demonstrated by several researchers (Gulati, 1983; Andronikova, 1996; Jeppesen et al., 1999, 2005; Haberman and Laugaste, 2003; Blank et al., 2010). The BZp/BPhyt was proposed by P. Nõges and T. Nõges (2006) as an indicator of the ecological status for Lake Peipsi, and class boundaries were developed (reference state −>3, high status 1–3, good 0.6–1, moderate 0.3–0.6, poor 0.1–0.3, bad <0.1). Taking into account these boundaries, Lake Peipsi s.s. in August can be classified as poor, while Lake Pihkva is even within the bad category. There were significant differences in the content of nutrients and characteristic features in the plankton revealed between the lake parts, showing different levels of trophy.
The results of the researchers mentioned above, and also this current study, have confirmed that the BZp/BPhyt ratio can be used as a marker criterion in the evaluation of the trophy of the body of water and its ecosystem. It has been demonstrated by several researchers that the mean zooplankton weight, especially that of cladocerans, decreases with the increasing trophic state of a body of water (Andronikova, 1996; Haberman and Künnap, 2002; Haberman and Laugaste, 2003; Jeppesen et al., 2000). Table 1 shows that in the hypertrophic Lake Pihkva the zooplankters were markedly smaller in size than these in the eutrophic Lake Peipsi s.s. The reduction of cladoceran weight in Lake Pihkva was caused largely by the higher abundance of the small-bodied (6–7 μg) Chydorus sphaericus Müller in this lake part, as compared with Lake Peipsi s.s. The cause for a lower mean weight of copepods in Lake Pihkva is the lower abundance of large-bodied (♂ −40 μg, ♀ −59 μg) Eudiaptomus gracilis (Sars) in this lake, as compared with Lake Peipsi s.s. The lower mean rotifer weight in Lake Pihkva was associated with the relatively high abundance of several especially small-bodied species, characteristic of highly eutrophic waters: - Keratella tecta (Gosse) −0.1 μg, Trichocerca rousseleti (Voigt) −0.03 μg, and T. similis (Wierzejski) −0.3 μg. Even the particularly small Anuraeopsis fissa (Gosse) −0.02 μg, an indicator of high trophy levels, has been found in Lake Pihkva, while it is not yet present in Lake Peipsi s.s.
In our study, the abundance of Ch. sphaericus in hypertrophic Lake Pihkva was found to be almost five times greater of that in the eutrophic Lake Peipsi s.s (Table 1). The small-bodied Chydorus sphaericus is often used as an indicator of eutrophic conditions (Pejler, 1983; De Eyto, 2001; Haberman and Virro, 2004); its abundance increases with the trophy level of a body of water. This cladoceran feeds mainly on detritus and on bacteria attached to detritus particles. Its share of the cladoceran group abundance was 37% in Lake Peipsi s.s., but 67% in Lake Pihkva. Ch. sphaericus was seen to be one of the dominant zooplankters (20% or more of whole zooplankton abundance) in Lake Pihkva, while this has not yet occurred in Lake Peipsi s.s.
The cladoceran Daphnia cucullata Sars, which has also been considered to be a species of eutrophic waters (Haberman and Virro, 2004), in Lake Peipsi seems not to be so closely related to eutrophy as does Ch. sphaericus. Species in the genus Daphnia are not very fastidious about food and are able to consume food objects of differing sizes (including bacteria), which gives them an advantage as filtrators (Kamjunke et al., 1999). As the species of Daphnia are effective consumers of algae and a favourite food item for fish, they are often considered the keystone species in freshwater ecosystems (Jeppesen et al., 1999; Kamjunke et al., 1999), and their indicative value in assessing the ecological state of waterbody is high.
The calanoid copepod Eudiaptomus gracilis is a zooplankter of oligo-mesotrophic waters (Andronikova, 1996; Haberman and Virro, 2004). In recent times, the abundance of this species in Lake Peipsi has decreased substantially. In 1997–1999 its mean abundance for the growing season was 11,000 ind m−3, while in 2004–2006 there were only 6,000 ind m−3. The selective feeding of E. gracilis mainly on small algae, may allow this species to be used as an indicator species, as it does not thrive in highly eutrophic waterbodies in which small algae are usually not abundant (Lampert, 1992). It has almost entirely disappeared from hypertrophic Dutch lakes (Gulati, 1983), and from hypertrophic Lake Võrtsjärv (Haberman and Virro, 2004), and its abundance has decreased from 17% of the entire zooplankton population to 2% even in the meso-oligotrophic Lake Ladoga (Andronikova, 1996).
The predominance of rotifers and their increasing proportion in an eutrophic waterbodies accompanying the eutrophication process is a well-known phenomenon (Gulati, 1983; Haberman and Virro, 2004). Recently, the abundance of rotifers in Lake Pihkva has decreased, what seemed to be caused by a massive poisonous cyanobacterial blooms in the lake (Haberman et al., 2010). According to Tanner et al. (2005), in Lake Peipsi s.s., the concentration of microcystins at a depth 30–50 cm was 50 μg l−1 in the open area and up to 1074 μg l−1 in the nearshore area at the beginning of September 2002. The dynamics of abundances of Keratella cochlearis (Gosse) and Polyarthra luminosa Kutikova (Table 1), rotifer species characteristic for eutrophic waters, in different parts of Lake Peipsi could also be explained by the presence of algal toxins. Rotifer species Keratella tecta and Trichocerca rousseleti have been shown by others to be indicators of high eutrophy (Duggan et al., 2001; Haberman and Virro, 2004), while Kellicottia longispina (Kellicot) is a species of oligo-mesotrophic waters (Hofmann and Höfle, 1993; Haberman and Virro, 2004). This has also been supported by our study (Tables 1 and 2). When selecting the indicators these zooplankton are widely accepted as appropriate for determining trophic status and ecological quality of lakes.
Our study has demonstrated statistically significant variances in the hydrochemistry and zoo- and phytoplankton data between the lake parts. Different natural conditions (topography, catchment area, relative depth) and different pollution loads in the lake parts have resulted in apparently different resistances in their ecosystems and different responses to human activity. At present, on the basis of TP data (up to 200 mg m−3), Lake Pihkva appears to act as a polluter of adjacent lake part, rather than a purification pond. In the past, when the TP content was lower (the mean 62 mg m−3 in 1985–1996) the lake evidently acted also as a purification pond for the whole lake.
This research was supported through targeted financing by the Estonian Ministry of Education research (project SF 0170006s08) and the Estonian Science Foundation (grant 7643). Hydrobiological collections from the Centre for Limnology and data from the Estonian State Monitoring Programme have been used. The contribution of the referees is highly appreciated.