Biologia, Bratislava, 62/6: 657—663, 2007 Section Botany DOI: 10.2478/s11756-007-0128-y

Habitat requirements of the Charetum intermediae phytocoenoses in lakes of western Poland

Maciej G˛abka1, PawelM.Owsianny2, Lubomira Burchardt1 &TadeuszSobczynski´ 3

1Adam Mickiewicz University, Department of Hydrobiology, Umultowska 89,PL-61–614 Pozna´n, Poland; e-mail: [email protected] 2Adam Mickiewicz University, Department of Geomorphology, Dzi˛egielowa 27,PL-61–680,Pozna´n, Poland 3Adam Mickiewicz University, Department of Water and Soil Analysis, Drzymaly 24,PL-60–613 Pozna´n, Poland

Abstract: The study presents habitat and phytosociological analyses of the Chara intermedia phytocenoses, rare described in Europe. 16 physico-chemical water parameters were analysed, coming from the samples taken in 20 phytocenoses of 13 lakes located in western Poland. The analysed community appeared in naturally shallow lakes representing last stages of the disappearance of glacial water basins. The study attempts to estimate the bioindicative value of the charophyta meadow Charetum intermediae in relation to its habitat. A particular attention has been paid to the determination of the habitat trophic condition, and to the concentration of elements connected with the hardness of water and the content of humic substances. The study shows crucial habitat gradients of the C. intermediae association, taking into account also the species composition of phytocenoses. Key words: Chara intermedia; Charetum intermediae; Characeae; habitat requirements; indicator value; macrophytes; water properties

Introduction Charophyte communities are usually interpreted as pioneering stages of lake bottom succession, as they Due to their close connection with lakes characteris- tend to occupy the deepest, organic parts of phy- tic of low trophy (Krause 1981; Blindow 1992; van der tolittoral (D˛ambska 1966; Krause 1981; Matuszkiewicz Berg et al. 1999), charophyta meadows are treated as 2001; Kufel & Kufel 2002 and references there; Ciecier- specific indicators: their presence in water basins is in- ska et al. 2003). However, in the case of glacial lakes terpreted as an element stabilising the ecosystems (e.g. developed in the process of succession, the data describ- Scheffer & Jeppesen 1998; Sheffer 2001; Ciecierska & ing charophytes and their habitat conditions are very Dziedzic 2003; Ciecierska et al. 2003). In the so-called scarce. charophyta lakes, the species of the Characeae family The aim of study was to characterize environ- are a dominating group of plants and may function as a mental conditions charophyte meadows of Charetum long-term plant phase limiting the development of other intermediae (Corillion 1957) Fijalkowski 1960 phy- macrophytes and phytoplankton (Ozimek 1992). tocoenoses from natural, shallow, mid-forest lakes Habitat numerical data describing the appearance in western part of Poland. Chara intermedia is a of charophytes, especially referring to the concentra- rare species in Poland and its phytocenoses were tion of nutrients and to light conditions, have already found in few localities only (D˛ambska 1966; Kar- been presented on a number of occasions (e. g. Ozimek czmarz & Malicki 1971; Tomaszewicz 1979); there- & Kowalczewski 1984; Blindow 1992; van den Berg et fore, this sub-cosmopolitan species was included in al. 1999; van Donk & van de Bund 2002; Kufel & Kufel the “Red list of the algae in Poland” (Siemi´nska 2002). What they tend to concentrate on is the determi- et al. 2006). In the Wielkopolska region, its com- nation of the relationships between habitat-community munity, Charetum intermediae, is considered as nat- and community-habitat. Still, it seems equally essen- ural, seriously endangered (category: V), and, until tial to study the relationships between phytoplancton now, relatively little known (Brzeg & Wojterska 2001). and charophytes, as they imply the theory of alterna- In Poland, the occurrence of the phytocenoses with tive stable states in shallow lakes (Scheffer & Jeppesen Chara intermedia is limited basically to hollow peat- 1998; Sheffer 2001). A correct determination of these bog ponds and astatic basins. The associations of relationships might help in phytoindication, as it might this macroalga were also recorded in a small num- use charophytes and their communities as indicators of ber of shallow lakes (D˛ambska 1966; Tomaszewicz progressing eutrofication (Ozimek 1992). 1979).

c 2007 Institute of Botany, Slovak Academy of Sciences 658 M. G˛abka

16o E 20o E 24o E

o 54 N 54o N

12 13 8-11 Vistula River 7

6 4 2-3 5 1 Oder River Poznañ Warsaw 52o N 52o N

Krakau 50o N 50o N

16o E 20o E 24o E

Fig. 1. Locations of the studied lakes

Study area and methods 10–20%; + – species present in 5–10% and r – species oc- curring in 0–5%. The study analysed the phytocenoses of Charetum inter- Plant names are those used by Mirek et al. (1995), mediae present in 13 small (< 10 ha), natural and mostly charophytes by Krause (1997) and the nomenclature of syn- very shallow lakes (< 3 m max. depth) situated in the taxa follows Brzeg & Wojterska (2001). Wielkopolska – and Southern Pomerania Lakelands in west- For each phytocenosis phytosociological records were ern Poland (Kondracki 1998). Those lakes are placed in taken, together with water samples coming from the mean forests with domination of coniferous type of forest, white depth of the vegetation plot. Each of the analysed water mostly large participation of Sphagnum transitional bogs samples consisted of three samples taken from the cen- in drainage basin. The basins were strongly shallowed and tral part of each patch (Klosowski & Tomaszewicz 1993; filled with half-liquid gyttja bottom sediments. They were Klosowski 1999). dominated by charophyta meadows overgrowing the water Physico-chemical analysis were performed according to mass up to the surface. The study was conducted in the the Siepak (1992) and Hermanowicz et al. (1998) standard following lakes, where sites (or groups of sites) with the methods. 16 physical-chemical parameters of water were charophyta meadows of Charetum intermediae were desig- analyzed: colors (platinum-cobalt standard method), trans- nated (with number of records): Kociolek (2), Czarne Male parency (by Secchi disc), acidity (pH) (with pH-meter), dis- (1), Modre (1), Zamorze (1), Ostrowo (1), Mnich (3), Swi˛´ ete solved organic carbon (DOC, with organic carbon analyzer), + (1), Ku´znik Maly (4), Ku´znik Du˙zy (2), Ku´znik Olsowy (1), NH4 (by Nessler’s colorimetric method), conductivity (EC), − Ku´znik Bagienny (1), Linowe (1) and Smolary (1). Loca- oxygen concentration (electrometric method), NO3 (by cad- 3− tions of studied lakes are shown in Figure 1. mium reduction method), PO4 (by the colorimetric ascor- 2− − Habitat and phytosociological analyses were made in bic acid method), SO4 (by nephelometric method), Cl summer during the period of maximal growth in the years (by Mohr’s argentometric method), Ca2+,Mg2+ (wersenian 2001–2005. Phytosociological records were prepared accord- method) Na+,K+ and total Fe (by atomic absorption spec- ing to the Braun-Blanquet method (Braun-Blanquet 1951). trometry method). The following parameters were measured The floristic composition under study were contained in one in the field: pH, water temperature, conductivity, dissolved synthetic table of shortened form. Abundance, constancy oxygen and oxygen saturation. The remaining ones were and coefficient of cover were worked out. Abundance was de- measured in laboratory. termined according to a modified six-degree scale by Braun- Considering the wide gradient we used the canonical Blanquet. Constancy was determined according to the fol- correspondence analysis (CCA, the method assuming uni- lowing scale on basis of the species abundance: V – species modal relation of species and environment) for the investiga- occurring in 80–100% of relevés taken in the pytocoenoses; tion of relation of particular species to environment. Conse- IV – species present in 60–80%; III – species present in 40– quently, detrended correspondence analysis was applied for 60%; II – species present in 20–40%; I – species present in the description of ecological gradient size (beta-diversity) Habitat requirements of Charetum intermediae phytocoenoses 659

(ter Braak & Šmilauer 1998). Table 1. Synoptic table of 20 phytosociological relevés of Chare- Forward selection procedure was used to reduce num- tum intermediae from the studied lakes of western Poland. ber of environmental variables by means of Monte Carlo Abundance permutation test with 999 permutations. Variables were re- Species Constancy moved until the level of significance p < 0.05 was reached. 5 4321+r

Ch. Charetum intermediae Chara intermedia 16 4 . . . . . V 100 Results Ch. Charetea fragilis: 1. Chara globularis . ...24. II30 Phytosociological characteristic of the Charetum in- Chara delicatula ...32.. II25 termediae phytocoenoses in natural lakes of western Chara tomentosa ...1.1.+10 Poland Nitellopsis obtusa . ...1.. r 5 The associations of Charetum intermediae were recor- Ch. Potametea: ded in 13 lakes; in 8 of them they created phyto- Nymphaea× borealis . ...21. I 15 cenoses dominating the vegetation within the limits Nymphaea alba ...11.. +10 of the water surface. The patches were located mostly Myriophyllum verticillatum . ....2. +10 in central parts of the basins. Sometimes, in consid- Accompanying species: erably shallowed lakes (max. up to 1 m deep), whose Utricularia vulgaris . ...17. II40 central parts were occupied by the phytocenoses with Utricularia minor . ....5. II25 Nymphaea × borealis (cross-breed forms of Nymphaea Stratiotes aloides . ...2.. I 10 alba s.s and Nymphaea candida), the charophyta mead- Typha latifolia . ....1. r 5 Phragmites australis . ....1. r 5 ows with Chara intermediae, in zone of vegetation, were Hydrocharis morsus-ranae . ....1. r 5 situated on the peripheries. It was only in the Zamorze Lemna minor . ....1. r 5 Lake where the Charetum intermediae appeared in a Typha angustifolia . ....1. r 5 small bay of the basin dominated by the patches of Nitellopsidetum obtusae. In four basins the vegetation plots were adjacent to the swamp part of the phytolit- toral. 2. Physical and chemical properties of water in Chare- The analysed charophyta meadows were poor in tum intermediate stands species, single-layered and considerably dense (Table 1). The charophyta meadows with Chara intermedia ap- For most cases Chara intermedia was created one- peared in strongly shallowed lakes with the dominat- species phytocenoses. Out of the 15 species recorded, ing habitat type based on substratum of calcium gyt- only Utricularia vulgaris, Utricularia minor, Chara tjas, strongly hydrated, and with a high concentration globularis and Chara delicatula reached the II degree of organic matter. The water depth of the Charetum of constancy. intermediae phytocenoses was mostly 1 m; only in the The vegetation plots dominated by Chara inter- Czarne Lake the patches present up to 3 m deep could media showed a wide spectrum of species ranging from be found. It has to be pointed out, however, that in characteristic for poor and rich waters, being a com- most of the cases the charophytes grew up to the very plex of transitions between moderate and hard aquatic water surface, and in some cases were even floating environment. CCA analysis revealed 3 groups. In the above the bottom without touching it. The habitats canonical correspondence analysis all the variables ex- of Charatum intermediae phytocoenoses were charac- plained 31% of the variation but not all the parameters terized with respect 16 water properties. Ranges and were significant (p < 0.05) in Monte Carlo permutation mean rates were contained in Table 2. test. The first group was floristically poor, single-species The charophyta meadows habitat is characteris- and connected with the deepest sites (1.5–3 m) located tic of high water colour and its humic nature, visi- in central parts of the basins. The second group of phy- ble in a considerable concentration of DOC. Despite tocenoses with Chara intermedia appeared in configu- the high water colour indices, the transparency of wa- rations with other charophyta species, e.g. Chara to- ter were reached to the bottom of the lakes. The con- mentosa, C. globularis, Nitellopsis obtusa,orwithsuch tent of humic substances in water was higher than that vascular plants as Stratiotes aloides,orMyriophyllum of most of the natural waters in the Wielkopolska re- verticillatum. In this group, among the accompanying gion (Baralkiewicz & Siepak 1994). The pH of water species it was Utricularia vulgaris which exhibited the ranged from slightly acidic to alkaline; in most cases, greatest constancy. Finally, the third group of phyto- however, it was about neutral. From numeric data it cenoses showed a characteristic presence of Chara del- mightfollowthattherecorded phytocenoses were con- icatula and Utricularia minor. In patches of shallow nected with meso- and eutrophic waters. They exhib- + − water, less than 0.5 m deep, especially in the third ited considerably high NH4 and NO3 contents and an group, some nympheids could be observed (Nymphaea average degree of water mineralization. The content alba and Nymphaea × borealis) or, sporadically, exam- of analysed nitrogen forms varied widely. The waters 3− + + ples of swamp vegetation such as Typha angustifolia, were poor in PO4 ,Na ,K , total Fe and, in most Typha latifolia and Phragmites australis. of the phytocenoses, in Cl−. The habitats of the Chara 660 M. G˛abka

1.0 Axis 2 Ca

EC Phraus SO4 Nymalb SD pH colour depht Lemmin Na O2 dissolved Utrvul Chaglo P-PO4 K Chaint Axis 1 Fe Nymbor Nitobt N-NH4 Typlat Chatom DOC Cl Stralo Myrver Utrmin Mg Chadel N-NO3

Typang Hydmor -0.6 -0.6 1.0

Fig. 2. CCA ordination of environmental variables and vegetation data of Charetum intermediae phytocoenoses. The eigenvalues of the first two axes are: 0.49 and 0.39. Species list: Chara intermedia (Chaint), Chara globularis (Chaglo), Chara delicatula (Chadel), Chara tomentosa (Chatom), Nitellopsis obtuse (Nitobt), Nymphaea × borealis (Nymbor), Nymphaea alba (Nymalb), Myriophyllum verticillatum (Myrver), Utricularia vulgaris (Utrvul), Utricularia minor (Utrmin), Stratiotes aloides (Stralo), Typha latifolia (Typlat), Phragmites australis (Phraus), Hydrocharis morsus-ranae (Hydmor), Lemna minor (Lemmin), Typha angustifolia (Typang).

Table 2. Depth of water, Secchi disc visibility (SD), physical and in the habitats of charophyta meadows were recorded chemical properties (see Methods for details) of water found in in lakes with strongly developed surrounding parts of habitats of Charetum intermediate. transitional peat-bogs. Property Range Mean Figure 2 presents the relationships between habi- tat variables and the species constituting the Chara in- Depth of water m 0.15–3.00 1.01 termedia charophyta meadows. Following stepwise se- SD m 0.15–2.00 0.91 Colour mg Pt L−1 6.00–86.00 36.85 lection (Monte Carlo permutation test) among 16 pa- DOC mg C L−1 5.30–26.46 13.21 rameters, 5 quantitative environmental variables turned pH 6.80–7.80 7.31 out to be significant: Ca2+,Cl−,Mg2+, colour of water −1 O2 dissolved mg O2 L 3.94–12.20 7.41 and dissolved oxygen. In forward selection procedure conductivity µScm−1 176.00–556.00 402.55 + −1 the remaining variables explained 57% of variation in N-NH4 mg N L 0.04–0.58 0.22 − −1 the species data. N-NO3 mg N L 0.00–0.50 0.13 3− −1 The first axis is to a large extent correlated with P-PO4 mg PO4 L 0.00–0.20 0.08 − + + Total Fe mg Fe L−1 0.00–0.12 0.04 Cl ,Na and K . These were the patches with the Ca2+ mg Ca L−1 24.51–102.11 47.78 participation of Chara tomentosa and Nitellopsis ob- 2+ −1 Mg mg Mg L 2.17–26.04 7.74 tusa that developed best in waters rich in these ele- Na+ mg Na L−1 1.03–16.32 4.78 K+ mg K L−1 0.23–5.20 1.03 ments. Worth noticing, too, is the distribution of most 2− −1 SO4 mg SO4 L 0.00–140.00 34.50 of the species along the other axis. We may conclude, − −1 2+ 2− Cl mg Cl L 4.00–70.00 11.7 then, that it is the presence of Ca and SO4 ,to- gether with conductivity, that seems to be decisive for n n = 20 (only for DOC – dissolved organic carbon = 18) the species configuration of the Charetum intermediae charophyta meadows. In the case of phytocenoses with habitats rich in Ca2+, we could observe an additional intermedia meadows were characteristic of high water participation of such species as Chara globularis, Utric- oxygenation. The Charetum intermediae phytocoenoses ularia vulgaris and Nymphaea alba. The waters of these 2+ 2+ 2− showed a wide range of Ca ,Mg and SO4 con- species were also, to some extent, coloured and poor 2+ − + tent. The content of Ca was characteristic of soft in NO3 and NH4 .ItwasthepresenceofUtricularia and medium-hard waters. Smaller values of elements minor and Chara delicatula in the patches of Charetum connected with the concentration of Ca2+ and Mg2+ intermediae that served as an indicator of the habitats Habitat requirements of Charetum intermediae phytocoenoses 661 poor in Ca2+. The patches with the presence of these stances flowing from the immediate catchment basin, species developed better in more highly coloured habi- is an important factor shaping habitat conditions of − + tats, richer in NO3 and NH4 . charophyta meadows with Chara intermedia. Factors connected with the concentration of Ca2+ Discussion have to be considered as the most important habitat pa- rameters shaping the occurrence of the analysed charo- In shallow, marcophytes-dominated lakes, charophytes phyta meadows. Charetum intermediae appeared both not only tend to occupy the habitats suitable for them, in waters rich in calcium compounds (alkaline) and in but they also influence their quality (van der Berg et those poorer in Ca2+ (with neutral reaction). It has to al. 1999; van Donk & van Bund 2002). Particularly, be pointed out that similar conclusions could be drawn they increase the transparency of water and lower its from earlier studies of Charetum intermediae,lessex- abundance in nutrients and calcium compounds, thus tensively documented with habitat data (Karczmarz & shaping the habitat conditions (Szefer 2001; Kufel & Malicki 1979; Krause 1981; Doll 1989). The appearance Kufel 2002). The relationship between the occurrence of of this syntaxon was usually connected with hard wa- charophytes and proper light and trophic conditions has ters rich in the Ca2+ compounds; less frequently was it been pointed out in a number of studies (e.g. Baszy´nski related to mid-bog lakes poorer in Ca2+. Chara inter- & Karczmarz 1997; Blindow 1988, 1992; van der Berg media grows primarily in shallowed lakes developed in et al. 1999). the process of succession (D˛ambska 1966; Karczmarz & On the basis of habitat analyses of charophyta Malicki 1979; Krause 1981; G˛abka 2004). meadows dominated by Chara intermedia we may ob- This study demonstrates that, in vegetation plots serve special relationships between the abiotic elements of the analysed meadow, it is the presence of the species important for the ecology of the Characeae. The zone of Utricularia minor and Chara delicatula that may be transitional peat-bogs, often of a considerable area, sur- interpreted as an indicator of habitats of charophyta rounding most of the lakes was a source of allochtonic meadow with small calcium content (with all its con- humic acids which exert a limiting influence on light sequences). In contrast, in the case of waters rich in conditions (e.g. Górniak 1996; Hutorowicz 2001), and calcium, it may be the presence of Utricularia vulgaris, thus prevent the charophytes from settling in the deep- Chara globularis and Nymphaea alba. est parts of this type of lakes (more than 3m deep). As far as the habitats of charophyta meadows with Therefore, Charetum intermediae occurred in shallow- Chara intermedia are concerned, in the case of lakes water conditions, overgrowing the water up to the water with strongly developed zones of surrounding peat- table. In deeper lakes, or on sites located in central parts bogs, the content of factors related to the hardness of of the basins, charophyta meadows were raised up to water was noticeably lower. We may suppose that, to- the water table. This position was connected with the gether with the development of peat-bogs, which serve physiological photosynthetic processes, as it provided as a biogeochemical barrier preventing the outflow of the macroalgae with proper light conditions (G˛abka Ca2+ to the basin, the domination of Charetum in- 2004). The presence of Charetum intermediae in shal- termediae in the lake may be an element responsible low basins can be interpreted as an indication of waters for the lowering of the hardness of water (G˛abka et al. rich in nutrients and humic acids, and classified some- 2004). It may result from the fact that the charophytes times as humotrophic waters. Taking into consideration use calcium compounds dissolved in water as a con- the internal floristic and habitat diversity of charophyta structive element of their thallus, and thus lower their meadows dominated by Chara intermedia,wecandis- concentration in water (Goldyn 1984; van der Berg et tinguish 2 groups of phytocenoses: (I) appeared on sites al. 1999; van der Berg et al. 2002). Therefore, charo- poor in Ca2+ andrichinnutrients,incontrasttothe phyta meadows with Chara intermedia play a crucial group (II), connected with hard waters, especially those role in the lowering of the hardness of water towards − + poorer in NO3 and NH4 . Both groups of phytocenoses the soft water conditions They tend to appear in the were rich in DOC and developed in coloured waters. habitats whose substrata are rich in calcium (G˛abka High content of nutrients found in well-lighted 2004; G˛abka et al. 2004), but whose concentration of shallow habitats of Charetum intermediae can be re- calcium in the water is considerably lower. lated to the periodic dissociation of humic acids and Charophytes are said to limit the development of the release of ammonium and phosphate ions into water phytoplancton, not only because of the competition for (e.g. Koenings & Hooper 1976; Franco & Heath 1982; nutrients, but also because their allelophatic impact Jones et al. 1988; Wojciechowski 1990; Wojciechowski (e.g. van Donk & van de Bund, 2002). This observa- & Górniak 1990). It is believed that the process of tion would imply the theory of alternative stable states photodegradation of the chelation connectionsof hu- and a number of intermediate unstable ones (Schef- mic acids and minerals compounds, observable in hard- fer 1989, 1990, 2001; Scheffer et al. 1993; Scheffer & water basins, is one of the factors influencing their eu- Jeppesen 1998). And indeed, this observation may be trophication (Jones et al. 1988; Wojciechowski 1990; confirmed by the analysis of the chlorophyll content in Wetzel 1992). That is why the phytocenoses with Chara the phytoplancton of the analysed lakes. As both the intermedia appeared in relatively eutrophic waters. On qualitative and the quantitative analyses of plancton the other hand, the constant supply of humic sub- algas coming from the habitats with Chara interme- 662 M. G˛abka dia demonstrated, in most of the cases we find a poor, Morska, May 19–22, 2005. Fund. Rozw. Uniw. Gda´nskiego, mesotrophic character of the phytoplancton, despite the Gda´nsk. habitats abounding in nutrients, resembling clear wa- G˛abka M. 2004. Wybrane aspekty siedliskowe wyst˛epowania ramienic w zarastaj˛acych jeziorach ´sródle´snych Wielkopolski, ter ones (G˛abka & Owsianny 2005). However, in some pp. 29–45. In: Burchardt L. (ed.), Zaslugi Prof. dr hab. Izabeli cases we could find a considerable biomass of phyto- D˛ambskiej w ksztaltowaniu dzisiejszego wizerunku ochrony plancton, despite the fact that C. intermedia occupied przyrody. Sesja naukowa w 20 rocznic˛e´smierci Prof. dr hab. almost the entire bottom of the analysed lakes. These Izabeli D˛ambskiej.UAM,Pozna´n. G˛abka M. Owsianny P.M. & Sobczy´nski T. 2004. Acidic lakes in examples might illustrate different variants of unstable the Wielkopolska region – physico-chemical properties of wa- states. Yet, in all of the lakes only a small participation ter, bottom sediments and the aquatic micro- and macroveg- of Cyanobacteria in phytoplancton could be detected. etation. Limnol. Rev. 4: 81–88. Goldyn H. 1984. Zbiorowiska ro´slin wodnych jeziora Zb˛echy This fact may confirm the alleged allelophatic effect of i okolicznych torfianek na Pojezierzu Leszczy´nskim. Bad. charophytes because their inhibiting impact was most Fizjogr. Polsk˛aZach.B36: 119–135. commonly noticed in the case of this particular group Górniak A. 1996. Substancje humusowe i ich rola w funkcjonowa- of algae (Berger & Schagerl 2004). niu ekosystemów slodkowodnych. Disserationes Universitatis Varsoviensis 448: 1–151. Therefore, we may conclude that the presence of Hermanowicz W., Do˙za´nskaW.,DojlidoJ.&KoziorowskiB. Charetum intermediae in very shallow, developed in the 1999. Fizyczno-chemiczne badania wody i ´scieków. Arkady, process of succession lakes of the Wielkopolska region, Warszawa, 847 pp. is a resultant of two factors: firstly, of light conditions, Hutorowicz A. 2001. Fitoplankton humusowego jeziora Smolak na tle zmian warunków fizyczno-chemicznych wywolanych wap- related to the concentration of humic substances and nowaniem i nawo˙zeniem. Idee Ekologiczne 14(7): 5–130. the possibility for charophyta meadows to grow up to Jones R.I., Salonen K. & de Haan H. 1988. Phosphorus transpho- the water table, and secondly, of the concentration of rmation in the epilimnion of humic lakes: abiotic interactions elements related to the hardness of water. between dissolved humic materials and phosphate. Fresh. Biol. 19: 357–369. Karczmarz K. & Malicki J. 1971. Zespoly i ekologia ramienic References PojezierzaL˛ eczy´nsko-Wlodawskiego. Annales Universitaties Mariae Curie-Sklodowska Lublin-Polonia. Sectio C. Vol. XXVI 23: 298–327. Baralkiewicz D. & Siepak J. 1994. The contents and variability of Klosowski S. & Tomaszewicz H. 1993. Standortsverh¨altnisse der TOC, POC and DOC concentration in natural waters. Polish Gesellschaften mit Dominanz einzelner Nymphaeaceen in J. Environ. Stud. 32: 1–15. Nordeost-Polen. Tuexenia 13: 75–90. Baszy´nski R. & Karczmarz K. 1997. Investigations on the produc- Klosowski S. 1999. Synecological studies on littoral vegetation in tion of inorganic matter of Charophya associations. 1. Fresh- northern Poland. Acta Hydrobiol. 41(6): 49–54. water associations. Acta Hydrobiol. 19(1): 1–7. Koenings J.P. & Hooper F.F. 1976. The influence of colloidal Berger J. & Schagerl M. 2004. Allelopathic activity of Characeae. organic matter on iron-phosphorus cycling in an acid bog Biologia 59: 9–15. lake. Limnol. Oceanogr. 21: 684–696. Blindow I. 1992. Decline of charophytes during eutrophication; a Kondracki J. 1998. Geografia regionalna Polski. Wyd. Nauk. comparison to angiosperms. Fresh. Biol. 28: 9–14. PWN, Warszawa, 440 pp. Braun-Blanquet J. 1951. Pflanzensoziologie. Springer Verlang, Krause W. 1981. Characeen als Bioindykatoren f¨ur den Gew¨as- Wien, 631 pp. serzustand. Limnologica 13(2): 399–418. Brzeg A. & Wojterska M. 2001. Zespoly ro´slinne Wielkopol- Krause W. 1997. Charales (Charophycae). S¨usswasserflora von ski, ich stan poznania i zagro˙zenie, pp. 39–110. In: Wo- Mitteleuropa, Band 18. Gustav Fischer, Jena, 202 pp. jterska M. (ed.), Szata ro´slinna Wielkopolski i Pojezierza Kufel L. & Kufel I. 2002. Chara beds acting as nutrient sinks in 72: Poludniowopomorskiego. Przewodnik sesji terenowych 52. shallow lakes – a review. Aquatic Bot. 249–260. Zjazdu PTB, 24–28 wrze´snia 2001, Pozna´n. Matuszkiewicz W. 2001. Przewodnik do oznaczania zbiorowisk Ciecierska H. & Dziedzic J. 2003. The occurrences of stoneworts ro´slinnych Polski. Wyd. Nauk. PWN, Warszawa, 537 pp. in the lakes located in the city of Olsztyn. In: Holdy´nski Cz. Mirek Z., Pi˛eko´s-Mirkowa H., Zaj˛ac A. & Zaj˛ac M. 1995. Vas- cular plants of Poland. A cheklist. Pol. Bot. Stud., Guideb. &La´zniewska I. (eds), Algae and Biological State of Water. Ser. 15. PAN, Kraków, 330 pp. Acta Bot. Warmiae et Masuriae 3: 221–228. Ozimek T. & Kowalczewski A. 1984. Long-term changes of Ciecierska H., Dziedzic J. & Zurawska˙ J. 2003. Stabilizing role of the submerged macrophytes in eutrophic Lake Mikolajskie Charophyta – the example of some lakes from the Pomeranian (North Poland). Aquatic Bot. 19: 1–11. Lake District (NW Poland). In: Holdy´nski Cz. &La´ zniewska Ozimek T. 1992. Makrofity zanurzone i ich relacje z glonami w I. (eds), Algae and Biological State of Water. Acta Bot. jeziorach o wysokiej trofii. Wiad. Ekol. 38: 13–34. Warmiae et Masuriae 3: 229–239. Scheffer M. & Jeppesen E. 1998. Alternative stable states. In: D˛ambska I. 1966. Zbiorowiska ramienic Polski. Prace Komisji Bi- Jeppesen E., Søndergaard M., Søndergaard M. & Christof- 31: ologicznej, PTPN, Wydzial Matematyczno-Przyrodniczy fersen K. (eds), The structure role of submerged macrophytes 1–76. in lakes. Ecol. Stud. 131: 387–406. Doll R. 1989. Die pflanzengesellschaften der stehenden Gew¨asser Scheffer M. 1989. Alternative stable states in eutrophic freshwater im Norden der DDR. Teil I. Die Gesellschaften des offe- systems. A minimal model. Hydrobiol. Bull. 23: 73–83. nen Wassers (Charceen-Gesellschaften). Feddes Repertorium Scheffer M. 1990. Multiplicity of stable states in freshwater sys- 100(5–6): 281–324. tems. Hydrobiol. 200/201: 475–486. Franco D.A. & Heath R.T. 1982. UV-sensitive complex phospho- Scheffer M. 2001. Ecology of shallow lakes. Kluwer Academic rous: Association with dissolved humic material and iron in Publishers, 356 pp. a bog lake. Limnol. Oceanogr. 27(3): 564–569. Scheffer M., Hosper S.H., Meijer M.L., Moss B. & Jeppesen E. G˛abka M. & Owsianny P.M. 2005. Occurrence of charophytes in 1993. Alternative equilibria in shallow lakes. Trends Ecol. humic lakes of the Wielkopolska region on the background Evol. 8: 275–279. of light conditions and their interrelations with algal floristic Siemi´nska J., B˛ak M., Dziedzic J., G˛abka M., Grygorowicz P., composition, p. 33. In: Abstracts of XXIV International Sym- Mrozi´nska T., Pelechaty M., Owsianny P. M., Pli´nski M. & posium of the Phycological Section of the Polish Botanical So- Witkowski A. 2006. Red list of the algae in Poland, pp. 37–52. ciety, Toxic Cyanobacteria – problem of the future”, Krynica In: Mirek Z., Zarzycki K., Wojewoda W. & Szel˛ag Z. (eds), Habitat requirements of Charetum intermediae phytocoenoses 663

Red list of plants and fungi in Poland. W. Szafer Institute of van Donk E. & van de Bund W.J. 2002. Impact of sub- Botany, Polish Academy of Science, Kraków. merged macrophytes including charophytes on phyto- and Siepak J. (ed.) 1992. Fizyczno-chemiczna analiza wód i gruntów. zooplankton communities: allelopathy versus other mecha- UAM, Pozna´n, 193 pp. nisms. Aquatic Bot. 72: 261–274. Tomaszewicz H. 1979. Ro´slinno´s´c wodna i szuwarowa Pol- Wetzel R.G. 1992. Gradient-dominated ecosystems: sources and ski (Klasy: Lemnetea, Charetea, Potamogetonetea, Phrag- regulatory functions of dissolved humic organic matter in mitetea) wg stanu zbadania na rok 1975 Rozprawy Uniw- freshwater ecosystems. Hydrobiol. 229: 181–198. ersytetu Warszawskiego 160, Wyd. Uniw. Warsz., Warszawa, Wojciechowski I. 1990. The trends of lake evolution due to al- 324 pp. lochtonous humic substances. Seria Biologia (A. Mickiewicz van den Berg M.S., Coops H., Simons J. & Pilon J. 2002. A University, Pozna´n) 43: 87–89. comparative study of the use of inorganic carbon resources Wojciechowski I. & Górniak A. 1990. Influence of the brown hu- by Chara aspera and Potamogeton pectinatus.AquaticBot. mic and fulvic acids originating from nearby peat bogs on 72: 219–233. phytoplankton activity in the littoral of two lakes in Mid- van den Berg M. S., Scheffer M., Man Nes E. & Coops H. 1999. Eastern Poland. Verh. Internat. Verein. Limnol. 24: 295–297. Dynamics and stability of Chara sp. and Potamogeton pecti- natus.Hydrobiol.408/409: 335–342. Received April 3, 2006 Accepted July 16, 2007