G Model ARTICLE IN PRESS AQBOT-2700; No. of Pages 9 Aquatic Botany xxx (2014) xxx–xxx Contents lists available at ScienceDirect Aquatic Botany journal homepage: www.elsevier.com/locate/aquabot Site-dependent species composition, structure and environmental conditions of Chara tomentosa L. meadows, western Poland Mariusz Pełechaty a,∗ , Joanna Ossowska a , Andrzej Pukacz b , Karina Apolinarska c , Marcin Siepak c a Department of Hydrobiology, Faculty of Biology, Adam Mickiewicz University in Poznań, Umultowska 89, 61-614 Poznań, Poland Polish-German Research Institute, Collegium Polonicum, Adam Mickiewicz University in Poznań-Europa Universität Viadrina Frankfurt (Oder), Kościuszki 1, 69-100 Słubice, Poland c Institute of Geology, Faculty of Geographical and Geological Sciences, Adam Mickiewicz University in Poznań, Maków Polnych 16, 61-606 Poznań, Poland b a r t i c l e i n f o Article history: Received 26 July 2013 Received in revised form 16 June 2014 Accepted 28 June 2014 Available online xxx Keywords: Community ecology Chara tomentosa Charophyte Macrophyte Hydrochemistry a b s t r a c t In this study we investigated the relationships between charophyte abundance and water chemistry in four well vegetated lakes in western Poland differing in morphometry, catchment basin characteristics, and intensity of human pressure. Species composition and abundance (expressed as cover and, additionally, as PVI values, defined as per cent volume of water infested by plants) of vegetation patches dominated by Chara tomentosa L. were determined along with water physicochemical characteristics at nine permanent study sites monthly from spring through autumn. We hypothesised that the species composition of C. tomentosa meadows is lake-specific whereas the abundant growth is the cause rather than a response to water quality of the studied lakes. C. tomentosa formed dense swards in every studied vegetation patch, irrespective of water depth, with negligible contributions of vascular plants to species richness and abundance. Although 15 macrophyte species were identified in the studied meadows, including eight charophytes, C. tomentosa dominated throughout the growing season. Heterogeneity observed in the species composition and cover was site-specific rather than related to physicochemical differences among the lakes. PVI values were positively correlated with water temperature and pH, and negatively correlated with water conductivity, hardness and Ca2+ concentrations. The results indicate a preference for high water clarity by most charophyte species found in the studied patches and highlight the possible influence of charophyte meadows on water quality, primarily on solute content, hardness and, thereby, as a positive feedback, on water clarity. © 2014 Elsevier B.V. All rights reserved. 1. Introduction Charophytes (stoneworts, Charophyta) are submerged macroscopic green algae which include extant (Characeae family, six genera world-wide) and fossil members of the order Charales. Charophytes live in direct contact with their aquatic environment, not only through their delicate rhizoids but also through their above-bottom parts, primarily the well-developed thallus. This direct contact makes them highly sensitive to changes in water quality. Therefore, although charophytes are well distributed all over the world and occur in various types of aquatic ∗ Corresponding author. Tel.: +48 61 8295760. E-mail addresses: marpelhydro@poczta.onet.pl (M. Pełechaty), jkrupska@poczta.onet.pl (J. Ossowska), andrzejpukacz@wp.pl (A. Pukacz), karinaap@amu.edu.pl (K. Apolinarska), siep@amu.edu.pl (M. Siepak). environments at sites along a wide depth gradient (e.g., Krause, 1997; Martin et al., 2003), they decrease proportionally as the degree of trophy increases (e.g., Ozimek and Kowalczewski, 1984; Blindow, 1992a; Schubert and Blindow, 2003). The abundant occurrence of most charophytes is limited to water bodies with clear, alkaline waters and low nutrient budget, and, hence, a decline of charophytes commonly indicates increasing trophic state (Hutchinson, 1975; Krause, 1981, 1997; Piotrowicz et al., 2006). Where growing abundantly, charophytes may play a special role in nutrient cycles and the maintenance of a clear-water state in shallow lakes. It is assumed, therefore, that well developed charophyte vegetation may actively affect the environmental conditions of the water bodies in which it occurs. Existing knowledge of the complex network of interactions in aquatic ecosystems involving charophytes justifies the current use of these macrophytes and their communities (charophyte meadows) as sensitive indicators http://dx.doi.org/10.1016/j.aquabot.2014.06.015 0304-3770/© 2014 Elsevier B.V. All rights reserved. Please cite this article in press as: Pełechaty, M., et al., Site-dependent species composition, structure and environmental conditions of Chara tomentosa L. meadows, western Poland. Aquat. Bot. (2014), http://dx.doi.org/10.1016/j.aquabot.2014.06.015 G Model AQBOT-2700; No. of Pages 9 2 ARTICLE IN PRESS M. Pełechaty et al. / Aquatic Botany xxx (2014) xxx–xxx Fig. 1. Lake locations and bathymetry of the studied sites. T1–T3: Chara tomentosa patches studied; P1–P3: pelagic sites; L – Lake Lednica, J – Lake Jasne, ZP – Lake Złoty Potok, N – Lake Niesłysz. Each shaded depth contour represents 5 m; the scale bar refers to the lakes. of the ecological state of waters (Blindow, 2000; Pełechaty et al., 2006; Apolinarska et al., 2011 and references therein). Even though Chara meadows play a major role in the ecology of certain water bodies, the state of knowledge about charophyte communities in Central Europe, including Poland, is still incomplete, and the available data on their occurrence conditions, species composition and structure require verification. The dynamics of the relationships between charophyte meadows and the water quality characteristics throughout the growing season may be essential for understanding changes in this type of vegetation. Thus, the investigation of the interspecific relationships and habitat-biocoenosis interplay in a charophyte community, measured at monthly intervals, was the primary aim of this study. The meadows dominated by Chara tomentosa L. were chosen because they represent the most common group of charophyte communities in Polish and European freshwaters, and brackish waters of the Baltic Sea (Krause, 1997; Blindow et al., 2002; Torn et al., 2003; Torn et al., 2006; ˛ Pełechaty et al., 2007; Gabka, 2009; Guiry, 2014). We hypothesised that the species composition of C. tomentosa meadows is lakespecific whereas the abundant growth is the cause of rather than a response to the water quality of the studied lakes differing in morphometry, catchment basin characteristics, and intensity of human pressure. 2. Material and methods 2.1. Studied lakes The study was performed in four lakes with extensively developed charophyte vegetation located in western Poland (Fig. 1), three in the Ziemia Lubuska region (Lake Niesłysz, Lake Złoty Potok and Lake Jasne) and one in the Wielkopolska region (Lake Lednica). The lakes vary in terms of their morphometry (surface area, depth and shape of lake basin), their type of catchment basin and the intensity of human pressure, differences that are reflected in the physicochemical properties of their water (Table 1). Based on these differences, these lakes provide an opportunity to compare the structure and composition of Chara communities under varied environmental conditions. Out of the water quality properties listed in Table 1, Lake Lednica had higher solute content, hardness, calcium concentration and nutrient budget (particularly total nitrogen concentrations) than the other lakes. In addition, the lowest water transparency was observed in this lake. The smallest and shallowest Lake Jasne had the lowest nutrient concentrations and solute content (Table 1). This lake is characterised by the greatest water clarity and is a typical charophyte-dominated lake with extensive monospecific Chara meadows, covering up to 60% of the Please cite this article in press as: Pełechaty, M., et al., Site-dependent species composition, structure and environmental conditions of Chara tomentosa L. meadows, western Poland. Aquat. Bot. (2014), http://dx.doi.org/10.1016/j.aquabot.2014.06.015 G Model ARTICLE IN PRESS AQBOT-2700; No. of Pages 9 M. Pełechaty et al. / Aquatic Botany xxx (2014) xxx–xxx 3 Table 1 Morphometry, land use and physicochemical water characteristics of lakes in which Chara tomentosa meadows were studied (based on bulletins of the Regional Inspectorate of Environmental Protection in Zielona Góra and Poznań, Poland; Pełechaty et al., 2007 and references therein; Zieleniewski pers. communication, 2012 and unpublished data on TSI index in Lake Lednica). For each lake, physicochemical properties of water are given based on the summer samples collected monthly (June–August) during this study at three pelagic sites. Means ± standard deviations (first line) are followed by minimum and maximum values (second line). Unit Lake Lednica Lake Złoty Potok Lake Niesłysz Lake Jasne Surface area Mean depth Maximum depth Stratification Trophic state Lake type Catchment area Main land use ha m m – TSI – km2 – Secchi depth visibility m Water temperature ◦ Oxygen mg L−1 pH – Conductivity ␮S cm−1 TP mg L−1 TN mg L−1 Ca2+ mg L−1 Total hardness ◦ 341.4 7.0 15.1 Complete 49.3 Natural, outflow 38.0 Agricultural in 75% and recreational 2.3 ± 0.6 1.6–3.0 21.2 ± 1.9 19.1–23.8 10.8 ± 1.0 9.6–12.0 8.7 ± 0.1 8.6–8.8 794 ± 22 770–823 0.07 ± 0.01 0.05–0.08 15.6 ± 6.1 10.4–23.8 110.7 ± 4.0 100.7–115.3 20.9 ± 0.6 19.4–21.5 32.8 5.9 13.7 Complete 45.2 Natural, closed 3.8 Forests, recreational use limited 4.1 ± 1.5 3.1–6.5 20.8 ± 0.4 20.1–21.4 9.5 ± 0.6 8.7–10.2 8.4 ± 0.2 8.2–8.7 324 ± 12 313–341 0.25 ± 0.12 0.16–0.44 2.4 ± 0.3 2.1–2.9 56.3 ± 2.9 53.8–61.6 9.0 ± 0.4 8.6–9.7 486.2 7.8 34.7 Complete 44.3 Natural, outflow 56.24 Forests, agricultural and recreational 4.3 ± 1.1 2.7–5.6 20.3 ± 0.3 19.9–20.9 10.7 ± 0.9 9.7–12.2 8.6 ± 0.2 8.3–8.9 301 ± 13 285–319 0.1 ± 0.03 0.06–0.17 1.4 ± 0.2 1.1–1.6 47.9 ± 3.6 44.0–52.8 8.1 ± 0.5 7.5–8.7 15.1 4.3 9.5 Incomplete 44.1 Natural, closed 3.44 Forests, recreational use limited 5.4 ± 0.4 5.1–6.1 21.6 ± 1.7 19.2–22.9 9.2 ± 0,9 8.2–10.6 8.6 ± 0.2 8.2–8.8 211 ± 5 204–216 0.03 ± 0.04 0.03–0.04 1.0 ± 0.1 0.9–1.1 45.3 ± 1.0 43.9–46.2 7.1 ± 0.2 6.9–7.3 C dH lake area (Pełechaty et al., 2010). According to Carlson’s (1977) trophic state index, three of the studied lakes, Lake Jasne, Lake Złoty Potok (both are mid-forest lakes) and Lake Niesłysz (partly forested catchment basin) are mesotrophic, while Lake Lednica (with almost deforested catchment basin) is slightly eutrophic. All the studied lakes feature well developed macrophyte vegetation and extensive charophyte meadows dominated by C. tomentosa and Nitellopsis obtusa (Desvaux) J. Groves in Lake Niesłysz, C. tomentosa, N. obtusa and C. aspera (Deth.) Willd. in Lake Złoty Potok, C. tomentosa, C. rudis A. Br. and C. polyacantha A. Br. in Lake Jasne, and C. tomentosa, N. obtusa and C. contraria Kütz. in Lake Lednica. In the latter, charophyte vegetation recovered at the beginning of this century, after three decades of eutrophication. 2.2. Vegetation study The vegetation study was conducted at permanent, separate vegetation patches dominated by C. tomentosa on a monthly basis between June and late October 2008 in Lake Lednica, Lake Złoty Potok and Lake Niesłysz and between April and late October 2009 in Lake Jasne (depending on the degree of vegetation development). Although Lake Jasne was studied a year later than the other lakes, there was no risk that the weather conditions in both study years influenced the results. According to data obtained from the Institute of Meteorology and Water Management (IMGW) in Poznań, Poland, weather conditions in the region were comparable in both years and summer mean temperatures (June–September) reached 16.7 ◦ C in 2008 and 17.07 ◦ C in 2009. Three permanent study sites per lake were established in Lake Lednica (LT1, LT2 and LT3) and in Lake Jasne (JT1, JT2 and JT3), two in Lake Złoty Potok (ZPT1 and ZPT2), and one in Lake Niesłysz (NT1; Fig. 1). The number of sites studied was governed by the pattern of vegetation development. In Lakes Lednica and Jasne, C. tomentosa covered large areas and formed numerous charophyte stands. In Lakes Złoty Potok and Niesłysz, the number of C. tomentosa phytocoenoses was significantly lower than in the former lakes, and thus, the number of potential study sites was different. At each study site, the plant species composition and cover were determined with the use of Braun-Blanquet (1964) phytosociological relèves (records), 25 m2 in area. In each relève, all species were listed and the per cent area covered by each species was estimated according to the Braun–Blanquet scale (Table 2). Furthermore, the per cent volume of water infested by plants (PVI) was calculated at each study site as the product of the per cent coverage of the plants and their height divided by the depth at which the patch occurred. The species coverage reached up to 100% at each site. The depths of the sites ranged from 1 m to 2.5 m (1.5 m on an average). We used PVI because it can be easily calculated and it is visually intuitive (i.e., 0% = no macrophytes and 100% = the water column overgrown from the lake bottom to the surface). The PVI is an important indicator of the significance of the vegetation in the aquatic environment and is related to water quality (Canfield et al., 1984; Weaver et al., 1997; Valley and Drake, 2007; Sayer et al., 2010). 2.3. Water sampling Prior to water sampling, basic in situ physicochemical measurements of the water above the studied charophyte patches, including water temperature, oxygen concentration, conductivity and pH, were performed by means of portable field measurement Table 2 The relations between per cent cover of macrophytes in the field (in a phytosociological relève) and the Braun-Blanquet (1964) and van der Maarel (1979) scales. % of the relève area Braun-Blanquet scale van der Maarel scale <0.1% 0.1% ≤5% 5–25% 25–50% 50–75% 75–100% r + 1 2 3 4 5 1 2 3 5 7 8 9 Please cite this article in press as: Pełechaty, M., et al., Site-dependent species composition, structure and environmental conditions of Chara tomentosa L. meadows, western Poland. Aquat. Bot. (2014), http://dx.doi.org/10.1016/j.aquabot.2014.06.015 G Model AQBOT-2700; No. of Pages 9 ARTICLE IN PRESS M. Pełechaty et al. / Aquatic Botany xxx (2014) xxx–xxx 4 equipment, Elmetron CX-401 (Elmetron Sp. j., Zabrze, Poland) CyberScan 200 and CyberScan 20 (Eutech Instruments Europe BV, Nijkerk, The Netherlands), respectively. For further analyses under laboratory conditions, water samples were collected in 1 L plastic bottles, preserved with chloroform and stored in a refrigerator. Additionally, three sampling sites in each lake were situated in the macrophyte-free pelagic zone (Fig. 1), for which the basic physicochemical analyses were supplemented with Secchi depth visibility. At each pelagic sampling site, field measurements and water sampling were performed at a depth of 0.5 m. Analytical procedures and laboratory equipment applied to determine the basic anion and cation concentrations (nutrient speciation forms and calcium) in the water samples, as well as total hardness, alkalinity and total Kjeldahl nitrogen were described in details in Pełechaty et al. (2010) and Pełechaty et al. (2013a). In order to characterize water quality of the studied lakes, we used the Carlson trophy state index (TSI, Carlson, 1977), obtained from published (in lakes Jasne, Złoty Potok and Niesłysz, Pełechaty et al., 2007) and unpublished (Lake Lednica) results of earlier studies. In Table 1 we used TSI values calculated from all required components for the TSI, i.e. summer total phosphorus concentration, chlorophyll-a concentration and Secchi depth. Additionally, we calculated TSI values separately for Secchi depth visibility (TSISD) and for total phosphorus (TSITP) to illustrate the differences between water clarity and phosphorus availability in charophytedominated lakes. Fig. 2. PCA output for the physicochemical properties of waters from above the Chara tomentosa meadows studied monthly between spring and autumn. For Lake Lednica N = 15 (three sites, five sampling months for each site, June–October, 2008); for Lake Złoty Potok N = 10 (two sites, five sampling months for each site, June–October, 2008); for Lake Niesłysz N = 5 (one site, five sampling months for each site, June–October, 2008); for Lake Jasne N = 21 (three sites, seven sampling months for each site, April–October, 2009). Explanations: TP – total phosphorus concentration, hard. – total hardness, TN – total nitrogen concentration, cond. – conductivity, oxygen – oxygen concentration; 69.6% of the variance is explained by both axes. 2.4. Statistical approach To make the phytocoenotic data useful for statistical analysis, the per cent cover of plants, expressed in Braun-Blanquet scale (range from r to 5), was transformed into van der Maarel (1979) scale (range from 1 to 9), as described in Table 2. A multivariate ordination technique was applied to analyse the physicochemical variation among the lakes studied and, additionally, to evidence the differences in the composition and coverage of charophytes and higher plant species among the surveyed vegetation stands. On the basis of detrended correspondence analysis (DCA), which revealed the gradient length of species to be shorter than three standard deviations, Principal Component Analyses (PCA) was performed (Ter Braack and Šmilauer, 2002) using CANOCO 4.5 for Windows (Wageningen UR, Netherlands). Because the speciation forms of nutrients are interrelated, total nitrogen (TN) and total phosphorus (TP) were included in the multivariate analysis of physicochemical data. Also included was total hardness, which represents Ca2+ concentration and alkalinity, and conductivity, reflecting solute content. Prior to PCA, physicochemical water properties were standardised. Spearman rank correlation was applied to analyse the relationships between community PVI and environmental variables. Because data were not normally distributed and the number of samples was limited, the non-parametric test was used. For this analysis, the pH measurements were transformed to hydrogen ion concentrations. P < 0.05 was accepted as being statistically significant. STATISTICA 8.1 (StatSoft Inc., Tusla, OK, USA) software program was used. 3. Results 3.1. Water properties The physicochemical properties of the pelagic waters (Table 1) clearly distinguished Lake Lednica from the other lakes, among which no differences were observed. Total hardness, conductivity, calcium and total nitrogen concentrations were most responsible for the observed differences. PCA analysis of waters sampled from above the C. tomentosa stands gave an analogous result (Fig. 2) and emphasised that water hardness, solute content, and TN were highest above Chara stands in Lake Lednica throughout the growing season. No significant differences occurred in water chemistry among the other lakes. Overall, almost 70% of the variance was explained by the first and second PCA axes (Fig. 2). 3.2. The structure of C. tomentosa stands Although C. tomentosa was the primary component of the studied patches, other macrophytes, both charophyte and higher plant species (vascular plants and one moss species), were recorded at the studied sites (Table 3, Fig. 3). Within the charophyte group, N. obtusa and C. contraria were most common, whereas among vascular plants, Najas marina L. and Ceratophyllum demersum L. occurred most often (Table 3, Fig. 3). The number of species per patch ranged from two to nine (Table 3). The higher number of charophyte species, compared to vascular macrophytes (Table 3, Fig. 4), underlines the former’s significance for the structure and composition of the studied patches. Higher plant species occurred as single specimens in the patches. Thus, no vascular plant species appeared as a co-dominant with C. tomentosa. This was particularly evident in the least fertilized Lake Jasne, in which a negligible contribution of higher plants was recorded in C. tomentosa meadows (Table 3, Fig. 4). Relative to lake surface area, charophytes from Lake Jasne formed the largest meadows compared to other lakes. Also, the highest charophyte species richness was noted at one of the sites in this lake (JT2, Table 3), where all eight of the recorded species were charophytes. Despite the above-mentioned lake-dependency, species composition and cover seemed to be site- rather than lake-specific. In addition to the results presented in Table 3 and Fig. 4, the PCA of species composition and cover (Fig. 5) confirmed the heterogeneity among the studied C. tomentosa patches. From the charophyte Please cite this article in press as: Pełechaty, M., et al., Site-dependent species composition, structure and environmental conditions of Chara tomentosa L. meadows, western Poland. Aquat. Bot. (2014), http://dx.doi.org/10.1016/j.aquabot.2014.06.015 G Model ARTICLE IN PRESS AQBOT-2700; No. of Pages 9 M. Pełechaty et al. / Aquatic Botany xxx (2014) xxx–xxx 5 Table 3 Occurrence of charophytes, mosses and vascular plants at the studied sites. + species occurred, − species did not occur; for site descriptions, see Fig. 1. Sites Charophytes Chara tomentosa L. Nitellopsis obtusa (Desvaux) Groves Chara contraria Kütz. Chara filiformis Hertzsch Chara aspera (Deth.) Willd. Chara rudis A. Br. Chara globularis Thull. Chara polyacantha A. Br. Chara virgata Kütz. Mosses and vascular plants Fontinalis antipyretica L. Najas marina L. Ceratophyllum demersum L. Utricularia vulgaris L. Batrachium circinatum (Sibth.) Fr. Myriophyllum spicatum L. Potamogeton pectinatus L. Total LT1 LT2 LT3 ZPT1 ZPT2 NT1 JT1 JT2 JT3 + + + + − − − − − + + + − − − − − − + + + − − − + − − + + + + + − − − − + + + − + + − + − + + + + + − − − − + − − − − + − − − + + + + − + + + + + − − − − + − − − − + − + − − − 6 − − − − − − − 3 − + − + − − − 6 − + + − − − + 8 − − + − + + − 9 + + + − − − − 8 − − − − − − − 2 − − − − − − − 8 − − + − − − − 3 Fig. 3. The number of occurrences of macrophytes in the studied Chara tomentosa patches. Black – charophytes; grey – vascular plant and moss species. group, C. rudis, highly correlated with the first axis, C. aspera, appreciably related to the second axis and C. contraria, correlated with both axes, were primarily responsible for the variance observed. C. rudis not only differed significantly between the patches studied in Lake Jasne and those in the other lakes, but was also distinctive among the sites within Lake Jasne (some of the Lake Jasne sites are placed in the left-hand panel of the PCA biplot, Fig. 5). C. contraria, accompanied by two vascular plants, Najas marina and Utricularia vulgaris L., appeared to be a significant contributor to the patches studied in Lake Lednica (this being clearly reflected in Fig. 5) but occurred also in four other patches. Of nine studied patches, this species occurred in seven (Fig. 3) and was noted in all studied lakes (Table 3). Concerning both charophyte and higher plant species, the highest species diversity was observed primarily in the patches studied in Lakes Złoty Potok and Niesłysz (Table 3), sharing, with some patches from Lake Jasne, the same separated group in the third quadrant of the PCA biplot (Fig. 5). As a dominant charophyte in all patches, C. tomentosa was obviously of less importance in the explanation of variance that, overall, was 70% explained by the first and second PCA axes. C. tomentosa formed dense swards at every studied stand irrespective of water depth. Although the above-mentioned charophyte and higher plant species contributed to the studied patches, C. tomentosa strongly dominated all macrophytes at most of the sites. The species coverage of less than 60% was recorded only at site LT1 in late October and, during the whole study period, at JT1, where C. rudis developed extensively along with C. tomentosa and contributed significantly to patch coverage acting as a co-dominant. Also at site JT3, C. rudis achieved a significant coverage. This Please cite this article in press as: Pełechaty, M., et al., Site-dependent species composition, structure and environmental conditions of Chara tomentosa L. meadows, western Poland. Aquat. Bot. (2014), http://dx.doi.org/10.1016/j.aquabot.2014.06.015 G Model AQBOT-2700; No. of Pages 9 6 ARTICLE IN PRESS M. Pełechaty et al. / Aquatic Botany xxx (2014) xxx–xxx Fig. 4. Monthly numbers of charophyte and higher plant species in the studied Chara tomentosa patches. Boxes = mean ± standard error, whiskers = minimum and maximum. White = charophytes, grey = mosses and vascular plants. For site descriptions, see Fig. 1. contrasts with site JT2, where C. tomentosa developed extensively at the beginning of the growing season and where its coverage remained high until autumn, whereas other charophytes occurred as accompanying species. We tested the relationship between the PVI of the C. tomentosa community in Lake Jasne and the physicochemical properties of the water (Fig. 6). At all three study sites, PVI was significantly (P < 0.05) positively correlated with water temperature (r: 0.80; 0.76; 0.81 for Fig. 5. PCA output for charophyte and higher plant species composition and cover in nine Chara tomentosa patches studied in four lakes monthly between spring and autumn. Number of observations as in Fig. 2. 70% of the variation is explained by both axes. Smaller font was used for species of less importance in the explanation of variance. Please cite this article in press as: Pełechaty, M., et al., Site-dependent species composition, structure and environmental conditions of Chara tomentosa L. meadows, western Poland. Aquat. Bot. (2014), http://dx.doi.org/10.1016/j.aquabot.2014.06.015 G Model AQBOT-2700; No. of Pages 9 ARTICLE IN PRESS M. Pełechaty et al. / Aquatic Botany xxx (2014) xxx–xxx 7 Fig. 6. Correlations between the PVI (per cent volume infested by plants) values of Chara tomentosa communities and selected physicochemical properties of Lake Jasne water collected from above the patches. Different sites and seasons are marked. Legend in Fig. e refers to all figures. Water properties: a. water temperature, b. conductivity, c. water hardness, d. Ca2+ concentration, e. H+ concentration. JT1, JT2 and JT3, respectively, Fig. 6a) and negatively correlated with conductivity (r: −0.90; −0.95; −0.91, Fig. 6b), hardness (r: −0.90; −0.90; −0.81, Fig. 6c), Ca2+ (r: −0.84; −0.90; −0.91, Fig. 6d) and H+ (r: −0.62; −0.81; −0.61, Fig. 6e). A negative correlation for H+ means a positive relationship with the pH. 4. Discussion Physicochemical properties of pelagic (Table 1) and above charophyte waters (Fig. 2) reflect the differences between the trophic levels of the studied lakes. Trophy is clearly higher in Lake Lednica, which is subjected to more intense human pressure compared to the other lakes under study. In this more fertilised lake, charophytes, thought to act as sensitive bioindicators of nutrient-poor waters (Krause, 1981,1997; Blindow, 2000), surprisingly constitute a significant or even prevailing contribution to the well-developed macrophyte vegetation. This especially concerns large charophyte species such as C. tomentosa, which builds extensive communities in Lake Lednica. Large stonewort species (> 1 mm shoot diameter) are considered the most sensitive to decreasing water transparency and, among submerged macrophytes, they are the first to disappear with increasing trophic level (Ozimek and Kowalczewski, 1984; Blindow, 1992a). This indicates that, despite the lowest clarity in the group of studied lakes (Table 1), the water in Lake Lednica is sufficiently transparent to support the development of charophyte meadows. By contrast to Lake Lednica, Lake Please cite this article in press as: Pełechaty, M., et al., Site-dependent species composition, structure and environmental conditions of Chara tomentosa L. meadows, western Poland. Aquat. Bot. (2014), http://dx.doi.org/10.1016/j.aquabot.2014.06.015 G Model AQBOT-2700; No. of Pages 9 8 ARTICLE IN PRESS M. Pełechaty et al. / Aquatic Botany xxx (2014) xxx–xxx Jasne is characterised by the lowest fertility and greatest water clarity among the studied lakes. Therefore, it seems not surprising that, in addition to a significant share of the bottom surface overgrown by charophyte meadows, the highest species diversity in the group of charophytes is characteristic of this lake along with a negligible contribution of higher plants (Pełechaty et al., 2010). Similarly to Lake Jasne, the two other studied lakes, Lake Niesłysz and Lake Złoty Potok, also offer good environmental conditions (Table 3) for abundant development of submerged vegetation, including diverse charophyte meadows (Pełechaty et al., 2007). Although charophytes are generally known to be associated with clear water, low trophy and good ecological status, there are some controversies concerning the use of some stonewort species as bioindicators. In recent studies, some species and communities were recorded in lakes of higher trophy than had previously been reported (e.g. Blindow, 1992a; Pełechaty et al., 2006). This finding allowed researchers to assume that light conditions have a crucial influence on the occurrence of macrophytes, especially charophytes, rather than nutrient concentrations (Karczmarz, 1967; Pełechaty et al., 2006; Apolinarska et al., 2011 and references therein). This mechanism appears to be the case in Lake Lednica, where a trophic level that is higher than in the other studied lakes did not reduce the extensive charophyte meadows. The long-term presence of extensive Chara beds in Lake Lednica may reflect a strong influence of charophyte communities on their own habitat, primarily on high water transparency (the clear water effect is a result), via direct and indirect competitive interference with other producers, especially planktonic algae and Cyanobacteria, and the stabilisation of conditions that are favourable for the maintenance of charophyte meadows (e.g., van den Berg et al., 1998a; van Donk and van de Bund, 2002 and references therein; Mulderij et al., 2003; Mulderij, 2006 and references therein; Pełechaty et al., 2006; Apolinarska et al., 2011). Considering our results and the above-mentioned literature data we postulate that water clarity is of prime importance for the abundant development of charophytes. In our opinion, however, the relationship between abundant charophyte vegetation and water transparency has a positive feedback. Increasing water clarity leads to an increase in charophyte cover and biomass which, in turn, improve and stabilise clarity of water. In addition to Lake Lednica, where the trophic state index based on Secchi depth values (TSISD) may indicate lower trophy than nutrient budget (TSISD = 43 vs. TSITP = 67, max. summer values, unpublished data), this also seems to be the case for other studied lakes. In Lake Jasne and Lake Niesłysz TSISD values indicated very good light conditions (TSISD = 35 and TSISD = 36, respectively), and in Lake Złoty Potok (TSISD = 42) this value was comparable with Lake Lednica, whereas TSITP values were 57 in each of these three lakes (Pełechaty et al., 2007), emphasising the differences between TSITP and TSISD values as well as lower phosphorus availability compared to Lake Lednica. Our assumption regarding interdependency between water clarity and charophyte abundance is supported by the data provided for Lake Veluwemeer, The Netherlands, for which the above bidirectional relationship was proposed as a possible mechanism of an increase in water clarity that, due to van den Berg et al. (1998b), was associated with increasing charophyte cover, a reaction to earlier water quality (and clarity) improvement. Under lowered phosphorus concentrations and improved light conditions charophytes can even become a strong competitor of vascular plants and, due to density competition and nutrient interference, can negatively affect the performance of plants and, ultimately, replace them. This is the case for Lower Lake Constance, Germany, where charophytes, growing abundantly as a result of lake water re-oligotrophication, reduced areas covered previously by Myriophyllum spicatum L. (Richter and Gross, 2013). Alternatively, charophytes can co-occur with vascular plants, even those considered as eutrophic species and strong competitors of charophytes, such as Ceratophyllum demersum, jointly shaping the light conditions (Pełechaty et al., 2013b). Among the lakes studied, Lake Lednica had the highest calcium concentration and water hardness while Lake Jasne had the lowest values. As already mentioned, this shallow lake offers good conditions for the development of particularly extensive charophyte meadows, dominated by large species (namely C. tomentosa and C. rudis). Under such conditions, photosynthetic activity in dense charophyte stands can result in the demineralisation of ambient water, reflected especially in bicarbonate depletion (McConnaughey, 1997; McConnaughey and Whelan, 1997; van den Berg et al., 1998b; Kufel and Kufel, 2002). Heavy carbonate encrustation made up of approximately 60% CaCO3 by dry weight (Hutchinson, 1975), commonly precipitated on the charophyte thalli, is a visible effect of bicarbonate uptake during intensive photosynthesis (Raven et al., 1986). The above-cited average carbonate encrustation can be far higher (Pełechaty et al., 2013a and references therein), as is the case for Lake Jasne (unpublished data). Therefore, a decrease in conductivity, water hardness and calcium concentration with increasing PVI during the growing season (Fig. 6), might have been a result of photosynthetically-induced water decalcification. The negative relationship between PVI and H+ concentration seems to support the significance of photosynthesis for the above-mentioned relationships. A further outcome can be phosphorus co-precipitation with CaCO3 , emphasized lately in the literature as an additional mechanism of charophyte influence on surrounding waters (charophytes as a nutrient sink, as summarised by Kufel and Kufel, 2002; Kufel et al., 2013) that can contribute to the charophyte-induced increase of water clarity. In this context, it seems worth mentioning that Lake Jasne is characterized not only by the greatest but also by the most stable water clarity (Table 3). In phytosociological terms, a characteristic feature of charophyte communities is that they have a simple community structure, usually with only one dominant species. Typically, these communities develop as species-poor carpets, usually being monospecific stands or with minor, if any, contributions of other macrophyte species, and cover up to 100% of the stand surface (Mulderij, ˛ et al., 2007; Pełechaty et al., 2010). C. tomentosa com2006; Gabka monly forms such compact monospecific submerged meadows. However, it can also appear along with other charophytes, such as N. obtusa, C. rudis, C. hispida L., C. contraria and C. globularis ˛ 1964; Podbielkowski and Tomaszewicz, 1996; Krause, (Dambska, 1997; Kraska, 2009) as well as with vascular accompanying species, e.g., Myriophyllum spicatum, Potamogeton natans L., P. pectinatus L., U. vulgaris, Stratiotes aloides L. (Podbielkowski and Tomaszewicz, ˛ 1996) and nymphaeids (Gabka, 2009). In this context, the studied C. tomentosa stands may be considered species rich. The high coverage of the dominant species at all studied stands until the late autumn months may result from the fact that, generally, Chara spp. have a longer growing season than other aquatic macrophytes (Blindow et al., 2002; Fernández-Aláez et al., 2002). Furthermore, C. tomentosa, along with several other species of the genus Chara and some of Nitella, may, under favourable conditions, overwinter as a full-grown plant and resume growth in the follow˛ ing spring from the top nodes (Dambska, 1964; Blindow, 1992b), thus exhibiting less fluctuation in biomass during the growing season (Fernández-Aláez et al., 2002). In conclusion, the heterogeneity in species composition and cover, documented in this study, was site-specific rather than related to physicochemical differences among the lakes, thus contradicting our hypothesis. Additionally, although we only have correlative evidence, it is likely that abundant charophyte growth caused the observed differences in water chemistry rather than being a response to water quality. This emphasises the need for verification of the environmental requirements of individual Please cite this article in press as: Pełechaty, M., et al., Site-dependent species composition, structure and environmental conditions of Chara tomentosa L. meadows, western Poland. Aquat. Bot. (2014), http://dx.doi.org/10.1016/j.aquabot.2014.06.015 G Model AQBOT-2700; No. of Pages 9 ARTICLE IN PRESS M. Pełechaty et al. / Aquatic Botany xxx (2014) xxx–xxx charophyte species and communities to confirm their reliability as bioindicators (Pukacz et al., 2013). Considering a significant role of charophytes for community processes and ecosystem functions, and subsequently, their influence on water quality we postulate that these macroalgae are indicative of general good ecological status rather than just the nutrient content of the water, particularly when they form extensive meadows. Acknowledgements The authors would like to express their gratitude for all the Reviewers and Editors comments that helped in the manuscript improvement. We are also grateful to Professor Allan Chivas for checking the English language and valuable remarks. The Institute of Meteorology and Water Management (IMGW) in Poznań, Poland, is kindly acknowledged for providing the information on weather conditions in the studied years. The study was financed by the Polish Ministry of Science and Higher Education as project No. NN305 337534 and by the Dean of Faculty of Biology of Adam Mickiewicz University as project No. PBWB-05/2010. References Apolinarska, K., Pełechaty, M., Pukacz, A., 2011. CaCO3 sedimentation by modern charophytes (Characeae): can calcified remains and carbonate ␦13 C and ␦18 O record the ecological state of lakes? –a review. Stud. Lim. Tel. 5, 55–66. Blindow, I., 2000. Distribution of charophytes along the Swedish coast in relation to salinity and eutrophication. Internat. Rev. Hydrobiol. 85, 707–717. Blindow, I., 1992a. Decline of charophytes during eutrophication: comparison with angiosperms. Freshwater Biol. 28, 9–14. Blindow, I., 1992b. Long- and short-term dynamics of submerged macrophytes in two shallow eutrophic lakes. Freshwater Biol. 28, 15–27. Blindow, I., Hargeby, A., Andersson, G., 2002. Seasonal changes of mechanisms maintaining clear water in a shallow lake with abundant Chara vegetation. Aquat. Bot. 72, 315–334. Braun-Blanquet, J., 1964. Pflanzensozologie, Grundzüge der Vegetationskunde. 3. [Phytosociology. The Basis of Vegetation Science], 3rd ed. Springer, Wien-New York (in German). Canfield Jr., D.E., Shireman, J.V., Colle, D.E., Haller, W.T., Watkins, C.E.I.I., Maceina, M.J., 1984. Prediction of chlorophyll a concentrations in Florida lakes: importance of aquatic macrophytes. Can. J. Fish. Aquat. Sci. 44, 495–501. Carlson, R.E., 1977. A trophic state index for lakes. Limnol. Oceanogr. 22, 361–369. ˛ Dambska, I., 1964. Charophyta—Ramienice. Flora słodkowodna Polski T. 13. [Charophyta–Stoneworts. Freshwater flora of Poland, Vol.13]. Państwowe Wyd. Naukowe, Warszawa (in Polish). Fernández-Aláez, M., Fernández-Aláez, C., Rodríguez, S., 2002. Seasonal changes in biomass of charophytes in shallow lakes in the northwest of Spain. Aquat. Bot. 72, 335–348. ˛ Gabka, M., 2009. Charophytes of the Wielkopolska region (NW Poland): distribution, taxonomy and autecology. Bogucki Wyd. Nauk, Poznań. ˛ Gabka, M., Owsianny, P.M., Burchardt, L., Sobczyński, T., 2007. Habitat requirements of the Charetum intermediae phytocoenoses in lakes of western Poland. Biologia Bratislava, Section Botany 62, 657–663. Guiry, M.D. in Guiry, M.D. and Guiry, G.M., 2014. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org; searched on 21 January 2014. Hutchinson, G.E.A., 1975. Treatise on Limnology, Vol. 3: Limnological Botany. Wiley, Chapman and Hall, Ltd, New York - London. Karczmarz, K., 1967. Variabilité et distribution géographique de Lychnothamnus barbatus (Meyen) Leonh. [Variability and geographical distribution of Lychnothamnus barbatus (Meyen) Leonh.]. Acta Soc. Bot. Pol. 36, 431–439 (in French). Kraska, M., 2009. Roślinność wybranych jezior pojezierza lubuskiego i pojezierza sławskiego(stan z lat 1977-1981) [The plant vegetation of selected lakes of the Lubuskie and Sława lake districts (in the years1977-1981)]. Seria Biologia nr 78 Wyd. Nauk. UAM, Poznań (in Polish). Krause, W., 1981. Characeen als Bioindicatoren für den Gewässerzustand. [Charophytes as Bioindicators of Water Status]. Limnologica, Berlin (in German). Krause, W., 1997. Charales (Charophyceae). Süsswasserflora von Mitteleuropa, Band 18. [Charales (Charophyceae). Freshwater flora of Central Europe. Vol. 18.]. Gustav Fischer, Jena. Germany (in German). Kufel, L., Kufel, I., 2002. Chara beds acting as nutrient sinks in shallow lakes–a review. Aquat. Bot. 72, 249–260. 9 Kufel, L., Biardzka, E., Strzałek, M., 2013. Calcium carbonate incrustation and phosphorus fractions in five charophyte species. Aquat. Bot. 109, 54–57. Martin, G., Torn, K., Blindow, I., Schubert, H., Munsterhjelm, R., Henricson, C., 2003. Introduction to charophytes. In: Schubert, H., Blindow, I. (Eds.), Charophytes of the Baltic Sea. A.R.G. Gantner Verlag Kommanditgesellschaft, Ruggell, pp. 3–14. McConnaughey, T., 1997. Acid secretion, calcification, and photosynthetic carbon concentrating mechanisms. Can. J. Bot. 76, 1119–1126. McConnaughey, T.A., Whelan, J.F., 1997. Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci. Rev. 42, 95–117. Mulderij, G., 2006. Chemical warfare in freshwater, allelopathic effects of macrophytes on phytoplankton. Ph.D. thesis, Netherlands Institute of Ecology. The Netherlands. Mulderij, G., van Donk, E., Roelofs, J.G.M., 2003. Differential sensitivity of green algae to allelopathic substances from Chara. Hydrobiologia 491, 261–271. Ozimek, T., Kowalczewski, A., 1984. Long-term changes of the submerged macrophytes in eutrophic Lake Mikołajskie (North Poland). Aquat. Bot. 19, 1–11. Pełechaty, M., Apolinarska, K., Pukacz, A., Krupska, J., Siepak, M., Boszke, P., Sinkowski, M., 2010. Stable isotope composition of Chara rudis incrustation in Lake Jasne, Poland. Hydrobiologia 656, 29–42. Pełechaty, M., Pełechata, A., Pukacz, A., 2007. Flora I Roślinność Ramienicowa Na Tle Stanu Trofii Jezior Pojezierza Lubuskiego (Środkowo-Zachodnia Polska) [Charophyte Flora and Vegetation Against the Background of the Trophy State of Lubuskie Lake District, mid-Western Poland]. Bogucki Wyd. Nauk, Poznań. Poland (in Polish). Pełechaty, M., Pełechata, A., Pukacz, A., Burchardt, L., 2006. Interrelationships between macrophytes (including charophytes) and phytoplankton and the ecological state of lakes. Ecohydrol. Hydrobiol. 6, 79–88. Pełechaty, M., Pukacz, A., Apolinarska, K., Pełechata, A., Siepak, M., 2013a. The significance of Chara vegetation in the precipitation of lacustrine calcium carbonate. Sedimentology 60, 1017–1035, http://dx.doi.org/10.1111/sed.12020. Pełechaty, M., Pronin, E., Pukacz, A., 2013b. Charophyte occurrence in Ceratophyllum demersum stands. Hydrobiologia, http://dx.doi.org/ 10.1007/s10750-013-1622-6. Piotrowicz, R., Kraska, M., Klimaszyk, P., Szyper, H., Joniak, T., 2006. Vegetation richness and nutrient loads in 16 Lakes of Drawieński National Park (Northern Poland). Pol. J. Environ. Stud. 15, 467–478. Podbielkowski, Z., Tomaszewicz, H., 1996. Zarys hydrobotaniki [Introduction to hydrobotany]. Wyd. Nauk. PWN, Warszawa (in Polish). Pukacz, A., Pełechaty, M., Pełechata, A., 2013. The relation between charophytes and habitat differentiation in temperate lowland lakes. Pol. J. Ecol. 61 (1), 105–118. Raven, J.A., Smith, F.A., Walker, N.A., 1986. Biomineralization in the Charophyceae sensu lato. In: Leadbeater, S.C., Riding, R. (Eds.), Biomineralization in lower plants and animals. Clarendon, Oxford, pp. 550–557. Richter, D., Gross, E., 2013. Chara can outcompete Myriophyllum under low phosphorus Supply. Aquat. Sci. 75 (3), 457–467, http://dx.doi.org/10.1007/s00027-013-0292-9. Sayer, C.D., Davidson, T.A., Jones, J.I., 2010. Seasonal dynamics of macrophytes and phytoplankton in shallow lakes: a eutrophication-driven pathway from plants to plankton? Freshwater Biol. 55, 500–513. Schubert, H., Blindow, I. (Eds.), 2003. Charophytes of the Baltic Sea. A.R.G. Gantner Verlag Kommanditgesellschaft, Ruggell. Ter Braack, C.J.F., Šmilauer, P., 2002. CANOCO Reference Manual and User’s Guide to Canoco for Windows: Software for Canonical Community Ordination (version 4.5). Microcomputer Power, Ithaca, NY. Torn, K., Martin, G., Munsterhjelm, R., 2003. Chara tomentosa L. 1753. In: Schubert, H., Blindow, I. (Eds.), Charophytes of the Baltic Sea. A.R.G. Gantner Verlag Kommanditgesellschaft, Ruggell, pp. 131–141. Torn, K., Martin, G., Paalme, T., 2006. Seasonal changes in biomass, elongation growth and primary production rate of Chara tomentosa in the NE Baltic Sea. Ann. Bot. Fennici 43, 276–283. Valley, R.D., Drake, M.T., 2007. What does resilience of a clear-water state in lakes mean for the spatial heterogeneity of submersed macrophyte biovolume? Aquat. Bot. 87, 307–319. van den Berg, M.S., Scheffer, M., Coops, H., Simons, J., 1998a. The role of Characean algae in the management of eutrophic shallow lakes. J. Phycol. 34, 750–756. van den Berg, M.S., Coops, H., Meijer, M.-L., Scheffer, M., Simons, J., 1998b. Clear water associated with a dense Chara vegetation in the shallow and turbid Lake Veluwemeer, The Netherlands. In: Jeppesen, E., Søndergaard, M., Christoffersen, K. (Eds.), The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York, pp. 339–352. van der Maarel, E., 1979. Transformation of cover-abundance values in phytosociology and its effect on community similarity. Vegetation 39, 97–114. van Donk, E., van de Bund, W.J., 2002. Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquat. Bot. 72, 261–274. Weaver, M.J., Magnuson, J.J., Clayton, M.K., 1997. Distribution of littoral fishes in structurally complex macrophytes. Can. J. Fish. Aquat. Sci. 54, 2277–2289. Please cite this article in press as: Pełechaty, M., et al., Site-dependent species composition, structure and environmental conditions of Chara tomentosa L. meadows, western Poland. Aquat. Bot. (2014), http://dx.doi.org/10.1016/j.aquabot.2014.06.015