Ecological assessment of Great Lota Lake ( Turkey ) on the base of diatom communities

1 Department of Biology, Art and Science Faculty, Adiyaman University, Adiyaman 02000, Turkey. 2 The Laboratory of Biodiversity and Ecology, the Institute of Evolution, University of Haifa, Mount Carmel, Haifa 31905 Israel. 3 Department of Biology, Art and Science Faculty, Dumlupınar University, Kütahya, 43100, Turkey. 4 Department of Biology, Art and Science Faculty, Dumlupınar University, Kütahya, 43100, Turkey.


INTRODUCTION
Algae (especially diatoms) are useful indicators of water quality because of their rapid response to environmental changes (Kelly and Whitton, 1995;Lowe and Pan, 1996;Schneider et al., 2000;Prygiel et al., 2002;Rimet et al., 2004).Turkey has ca.900 natural lakes and ponds covering an area of over 10 000 km 2 .Many of these lakes have a high level of endemism among animals and plants owing to habitat and climate diversity and lack of major disturbances (Beklioğlu, 2010).Because the use of diatom indices and bio-indication in water quality monitoring is relatively new for Turkey, the investigations of the diatoms are important in these habitats for both ecological and taxonomical approaches.The aims of this study were to assess water quality dynamic, to observe changes in some biotic indices seasonally and to determine ecosystem performance statistically based on diatom community.
The environments and epiphytic diatom community of the lake were previously investigated by Sıvacı et al. (2008) by using redundancy analysis methods and the results show that there were strong correlation between diatom distributions and environmental variables such as temperature, Ca, TSP and SO 4 in the lake.

MATERIALS AND METHODS
Descriptive statistics of 14 variables are summarized in Table 1.Dissolved oxygen concentration (DO) and water temperature (YSI 51B Model), conductivity (Jenway 4070 Model) and pH (Orion 250-A Model) were measured in the field.Water for chemical analyses bottles, following filtration through GF/C filters for ammonium, Table 1.Species frequency according to 6-score scale according to Korde (1956).

Score
Visual Estimate Cell numbers per slide 1 Occasional 1-5 2 Rare 10-15 3 Common 25-30 4 Frequent 1 cell over a slide transect 5 Very frequent Several cells over a slide transect 6 Abundant One or more cells in each field of view nitrate and soluble reactive phosphorus determinations.Unfiltered water was used for other variables.All analyses were completed within 18 h of sampling.Alkalinity was determined by titration with HCI using BDH 4.5 indicator.Soluble reactive phosphorus (SRP), total soluble phosphorus (TSP), total phosphorus (TP), silicate (SiO 3 ), chlorine (Cl -), calcium (Ca 2+ ), sulphate (SO 4 2-) and ammonium (NH 4 + ) were determined according to Mackereth et al. (1978) to a precision of ± 4%.Nitrate was determined by reduction to nitrite on spongy cadmium and subsequent diazotization to a pink dye, determined spectrophotometrically, to a precision of ± 3%.
Measurements were taken from October 2000 to October 2001 in sampling periods of approximately every 15-day (no measurement available in February due to freezing), making up 19 samples from one station.Diatoms were collected by brushing from stones.Then, they were cleaned with HCl and H 2 O 2 for microscopic observation at a magnification of 1000X.After preparing three slides for samples, the diatoms were identified according to Krammer and Lange-Bertalot (1986;1988;1991a;b).Autecology and geographic distribution of the diatoms were compiled according to Hustedt (1939;1957), Sládeček (1986) and Watanabe et al. (1986).Ecological analyses were done based on the indicator species of Hustedt, Sládeček, Van Dam's systems,   (Barinova et al., 2006b).showing the status of pH, salinity, temperature, habitat preferences, streaming and oxygenation, organic pollution, N-uptake metabolism indicator species.The density scores were calculated by using the 6-score scale (Korde, 1956) (Table 1) for the saprobity index S. Also, the chronological types of the species were revealed according to Sládeček (1986) (Table 5).

Saprobity index (S)
The Saprobity Index (S) was calculated as: (1) Where, S is the index of saprobity for the diatom community; Si is the species-specific saprobity index and ai is the density score.S value, between 0 and 4 is the "weighted mean" of all individual indices that defines the self-purification zone corresponding to five classes of water quality (Sládeček, 1973) (Table 2).This bioindication approach is based on the ecological classification, which is widely used in European and Asian countries (Romanenko et al., 1990;Whitton et al., 1991;WFD, 2000).The classification of water quality in European systems is correlated with organic pollution level, salinity and tropic state assessment of aquatic ecosystems.

The aquatic ecosystem state index (WESI)
The index of ecosystem status (Aquatic Ecosystem State Index, WESI) is based on the water quality classes reflecting the self-purification capacities for each of the sampling stations or periods.It is calculated as: WESI = Rank S / Rank N-NO 3 (2) Where, Rank S is the rank of water quality based on the Sládeček indices of saprobity; Rank N-NO 3 is the rank of water quality based on the nitric-nitrogen concentration (Table 3).
If WESI is equal to or larger than 1, the photosynthetic level is positively correlated with the level of nitrate concentration.If the WESI is less than 1, the photosynthesis is suppressed presumably according to toxic disturbance (Barinova et al., 2006a;b;2010a;b).

Statistical data analysis
The relationship between species diversity (represented in each community) with environmental data can be used for climatehuman-environment interaction assessment (as well as saprobity index S) on the sampling stations.For this purpose, Canonical Correspondence Analysis (CCA) was conducted on the sensitivity of species to environmental variables for each sample using CANOCO Program (Statistica 7.0, StatSoft, 1996) (Ter Braak and Šmilauer, 2002).

RESULTS AND DISCUSSION
It should be noted that in natural freshwaters, the expected amount of sulphate is between 3 to 30 mg/L -1 and of calcium 6 to 78 mg/L -1 (Moss, 1973); the measured values of these ions in the Great Lota Lake were considered extreme, as the average values were above 250 mg.L -1 and 500 mg.L -1 for sulfate and calcium (Sıvacı et al., 2008) (Table 4).
Totally, 104 epilithic diatom species were found during the study (Table 5).Mastogloia spp.were the most dominant species and was followed by the taxa in decreasing magnitude of dominance; Gomphonema spp.(especially Gomphonema parvulum), Cymbella spp.(particularly Cymbella affinis), Caloneis spp.and Nitzschia spp. in the lake periphyton.Geographic ranges are known for 81 species from the Great Lota Lake; about 75.7% of the total species diversity.The chronological analysis reveals that most of the species were widespread or cosmopolitan (Table 5).There were 39 (54.9 %) indicator species for oxygenation while, there were only two species (Halamphora montana and H. normannii) of high oxygen level (Figure 2a).The assessments of organic pollution level based on Watanabe's system revealed 60 indicator species (57.7%) representing all the classes, but with a strong prevalence of eurysaprobionts (Figure 2b).The indicators of salinity (95 species; 91.3%) were assigned to four ecological groups arranged along the gradient of salinity.The numerous ones were the "indifferents" of a broad tolerance of salinity fluctuations (Figure 2c).Five groups of acidification indicators comprised 88 (84.6%) species (Figure 2d).On the diagram, these groups were arranged along the pH gradient.The ratio of the groups reflects the influence of carbonate substrates, and therefore alkaliphiles predominate, with 52 species (59.1%).The ''indifferents'', usually prevailing over silicate substrates, were subordinate here with 23 species.Alkalibiontes and acidophiles are represented by few species, but they are never abundant and acidophile species.The assessments of organic pollution level based on Sládeček's system, class II (oligosaprobic zone) and class III (betamesosaprobic zone) species were dominant in the community (36 species; 43.9% and 26 species; 31.7% respectively) (Figure 2e).The N-uptake metabolism indicators include 88 species (84.6%) representing four classes.The group "ats" of photosyntetically active species was significantly dominant in the community (Figure 2f and 2m).The indicators of trophic states revealed 65 species (62.5%).The most representative was eutraphenthic group (31 species) (Figure 2g).The diatoms in the lake inhabited all the available aquatic habitats of the water column, submerged substrates and wet rocky banks.On the diagram, the ecological groups were ordinated according to their relationships with the substrate, and it shows increase in species number.The benthic forms (68 species, 70.1%) prevailed, and the planktobenthic group (25 species, 25.8 %) was next in the species richness (Figure 2h).For temperature, there were 29 species (27.9% of all species).This is not enough for a detailed analysis, although the temperate species obviously prevailed (Figure 2k).
As seen in Figure 3, Species richness in diatom communities is strongly correlated with cells abundance over all investigated period.Both parameters were lower in the winter season whereas increased in summer from April to September when temperature and sunlight intensity were high.
impact; also, the fluctuation of the Index Saprobity and Class II of Water Quality, while the minimum at the end S reflects organic pollution affecting the community.The maximum index value was in winter (1.41), and the water was oligosaprobic; self-purification of summer was 1.08 (Tables 2, 3; Figure 4).The index value decreased over the study period as marked by the linear trend line.Its fluctuation can be also divided in the two periods.The value had the same fluctuation with species richness and cell abundance between April and September,  5.  whereas it had vice versa correlation from September to March.Therefore, species diversity and productivity of diatom communities of the Great Lota Lake are slightly influenced by increasing organic pollution during the autumn-spring period but is stimulated during the warmest summer period because the of the increase of photosynthetic activity (Figure 4).Regarding CCA analysis (Figure 5), there were four diff-erent groups.Group 1 was the group of N-NO 3 ; conductivity, and chlorides (left down circle) correlated with increasing species richness in communities and depended on anthropogenic influence that stimulates diversity increase.Indicator species was Pinnularia sudetica (Hilse) Hilse.Group 2 was the group of pH, DO, chlorophyll and index saprobioty S (left up circle) correlated with increasing organic pollution; mostly nutrients and depended on  on anthropogenic influence that stimulates community productivity.Indicator species were Surirella angustata Kütz.and Fragilaria sp.Group 3 was the group of phosphorous and silicates (right up circle) from the river bottom carbonates and correlated with natural influences.Indicator species was Neidium sp. which survived in the sediments only.Group 4 was the group of calcium and temperature that depended on climatic seasonal fluctuation.Indicator species could not be revealed.Groups 1 and 3 had antagonistic influence to diatom community, as well as groups 2 and 4. Therefore, species that were indicators for the variables group 1 were bio-sensing and alternative to the variables of group 3 and vice versa, indicators to the variables of group 2 were sensitive to the variables of group 4. In other words, organic pollution stimulated species diversity and biological productivity (left upper and lower triplot quadrants) of diatom community whereas the natural dependent variables (right upper and lower triplot quadrants) were not so impacted by the diatoms.Remarkably, the most abundant species (such as Fragilaria virescens, Gomphonema acuminatum, Caloneis subsalina and many others) had not specific correlations with the environmental variables of the lake.
We calculated Index WESI for diatom communities of the Great Lota Lake on the base of Index saprobity S and the classification of N-nitrate concentration from the ecological point of view (Barinova et al. 2006a).As a result, Figure 6 shows that the ecosystem of the lake was rather healthy with Index WESI more than 1 or slightly lower but not less than 0.75.The community was impacted in winter (December-January), May, and July.It correlated with periods of alternate correlations of species richness, abundance and Index saprobity S, which means that the lake communities were impacted by photosynthetic toxicants during winter, late spring, and peak of summer.These toxic substances can come from organic degradation processes in winter and from algal (usually cyanobacteria) bloom in summer (unpublished data).
In conclusion, totally, 104 diatom taxa were found in this study.Of these, 101 species are indicators of environmental conditions.The diatoms of the lake were low saline, alkaline characteristics and prefer temperate water.According to Watanabe's saprobity system, the lake was oligo-and betamesosaprobic and trophic state was eutrophic condition according to Van Dam's system.As a result, diatom community content is closely related with water quality, which helps for revealing critical periods for the ecosystems, and therefore bio-indicational methods can be used in the monitoring system in Turkey.

Figure 1 .
Figure 1.The location of Lake Great Lota in Turkey.

Figure 2 .
Figure 2. Bio-indication plot for the Great Lota Lake communities: a, oxygenation; b, organic pollution indicators (after Watanabe et al., 1986); c, salinity indicator group; d, acidification groups of indicator species; e, indicators of the Water Quality Class (after Sládeček, 1973); f, photosynthetic activity as a nitrogen uptake metabolism indicators (after Van Dam et al., 1994); g, trophic state indicator groups (after Van Dam et al., 1994); h, substrate preferences; k, temperature; m, dynamic of photosynthetic activity indicators.Symbols as in Table5.

Figure 3 .
Figure 3. Dynamic of Species richness and abundance of cells in diatom communities of the Great Lota Lake.

Figure 4 .
Figure 4. Dynamic of species richness and in diatom communities and Index Saprobity S of the Great Lota Lake.

Figure 5 .
Figure 5. Dynamic of species richness and in diatom communities and Index saprobity S of the Great Lota Lake.

Figure 6 .
Figure 6.Aquatic ecosystem state index WESI fluctuation in the Great Lota Lake.

Table 3 .
Water quality classification from ecological point of view

Table 4 .
Abbreviations and units of environmental variables with basic statistical summaries.Sample size n=19.

Table 5 .
The diatom indicators of environments in the Lota Lake with their autoecology and abundance scores in the communities.