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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 ´ski3 Maciej G˛ abka1, Pawe
l M. Owsianny2, Lubomira Burchardt1 & Tadeusz Sobczyn 1

Adam Mickiewicz University, Department of Hydrobiology, Umultowska 89, PL-61–614 Pozna´ n, Poland; e-mail: [email protected] 2 Adam Mickiewicz University, Department of Geomorphology, Dzi˛egielowa 27, PL-61–680, Pozna´ n, Poland 3 Adam Mickiewicz University, Department of Water and Soil Analysis, Drzyma
ly 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 Due to their close connection with lakes characteristic of low trophy (Krause 1981; Blindow 1992; van der Berg et al. 1999), charophyta meadows are treated as specific indicators: their presence in water basins is interpreted as an element stabilising the ecosystems (e.g. Scheffer & Jeppesen 1998; Sheffer 2001; Ciecierska & Dziedzic 2003; Ciecierska et al. 2003). In the so-called charophyta lakes, the species of the Characeae family are a dominating group of plants and may function as a long-term plant phase limiting the development of other macrophytes and phytoplankton (Ozimek 1992). Habitat numerical data describing the appearance of charophytes, especially referring to the concentration of nutrients and to light conditions, have already been presented on a number of occasions (e. g. Ozimek & Kowalczewski 1984; Blindow 1992; van den Berg et al. 1999; van Donk & van de Bund 2002; Kufel & Kufel 2002). What they tend to concentrate on is the determination of the relationships between habitat-community and community-habitat. Still, it seems equally essential to study the relationships between phytoplancton and charophytes, as they imply the theory of alternative stable states in shallow lakes (Scheffer & Jeppesen 1998; Sheffer 2001). A correct determination of these relationships might help in phytoindication, as it might use charophytes and their communities as indicators of progressing eutrofication (Ozimek 1992).

c
2007 Institute of Botany, Slovak Academy of Sciences

Charophyte communities are usually interpreted as pioneering stages of lake bottom succession, as they tend to occupy the deepest, organic parts of phytolittoral (D˛ambska 1966; Krause 1981; Matuszkiewicz 2001; Kufel & Kufel 2002 and references there; Ciecierska et al. 2003). However, in the case of glacial lakes developed in the process of succession, the data describing charophytes and their habitat conditions are very scarce. The aim of study was to characterize environmental conditions charophyte meadows of Charetum intermediae (Corillion 1957) Fija
lkowski 1960 phytocoenoses from natural, shallow, mid-forest lakes in western part of Poland. Chara intermedia is a rare species in Poland and its phytocenoses were found in few localities only (D˛ambska 1966; Karczmarz & Malicki 1971; Tomaszewicz 1979); therefore, this sub-cosmopolitan species was included in the “Red list of the algae in Poland” (Siemi´ nska et al. 2006). In the Wielkopolska region, its community, Charetum intermediae, is considered as natural, seriously endangered (category: V), and, until now, relatively little known (Brzeg & Wojterska 2001). In Poland, the occurrence of the phytocenoses with Chara intermedia is limited basically to hollow peatbog ponds and astatic basins. The associations of this macroalga were also recorded in a small number of shallow lakes (D˛ambska 1966; Tomaszewicz 1979).

658

M. G˛ abka 16oE

24oE

20oE

54oN

54oN

13 8-11

12 7 6 o

52 N

Ode r Riv er

5

4

2-3 1

Vi st ul a

Ri ve r

Warsaw

Poznañ

52oN

Krakau

50oN

20oE

16oE

50oN

24oE

Fig. 1. Locations of the studied lakes

Study area and methods The study analysed the phytocenoses of Charetum intermediae present in 13 small (< 10 ha), natural and mostly very shallow lakes (< 3 m max. depth) situated in the Wielkopolska – and Southern Pomerania Lakelands in western Poland (Kondracki 1998). Those lakes are placed in forests with domination of coniferous type of forest, white mostly large participation of Sphagnum transitional bogs in drainage basin. The basins were strongly shallowed and filled with half-liquid gyttja bottom sediments. They were dominated by charophyta meadows overgrowing the water mass up to the surface. The study was conducted in the following lakes, where sites (or groups of sites) with the charophyta meadows of Charetum intermediae were designated (with number of records): Kocio
lek (2), Czarne Ma
le ´ ete (1), Modre (1), Zamorze (1), Ostrowo (1), Mnich (3), Swi˛ (1), Ku´znik Ma
ly (4), Ku´znik Du˙zy (2), Ku´znik Olsowy (1), Ku´znik Bagienny (1), Linowe (1) and Smolary (1). Locations of studied lakes are shown in Figure 1. Habitat and phytosociological analyses were made in summer during the period of maximal growth in the years 2001–2005. Phytosociological records were prepared according to the Braun-Blanquet method (Braun-Blanquet 1951). The floristic composition under study were contained in one synthetic table of shortened form. Abundance, constancy and coefficient of cover were worked out. Abundance was determined according to a modified six-degree scale by BraunBlanquet. Constancy was determined according to the following scale on basis of the species abundance: V – species occurring in 80–100% of relevés taken in the pytocoenoses; IV – species present in 60–80%; III – species present in 40– 60%; II – species present in 20–40%; I – species present in

10–20%; + – species present in 5–10% and r – species occurring in 0–5%. Plant names are those used by Mirek et al. (1995), charophytes by Krause (1997) and the nomenclature of syntaxa follows Brzeg & Wojterska (2001). For each phytocenosis phytosociological records were taken, together with water samples coming from the mean depth of the vegetation plot. Each of the analysed water samples consisted of three samples taken from the central part of each patch (K
losowski & Tomaszewicz 1993; K
losowski 1999). Physico-chemical analysis were performed according to the Siepak (1992) and Hermanowicz et al. (1998) standard methods. 16 physical-chemical parameters of water were analyzed: colors (platinum-cobalt standard method), transparency (by Secchi disc), acidity (pH) (with pH-meter), dissolved organic carbon (DOC, with organic carbon analyzer), NH+ 4 (by Nessler’s colorimetric method), conductivity (EC), oxygen concentration (electrometric method), NO− 3 (by cad(by the colorimetric ascormium reduction method), PO3− 4 bic acid method), SO2− (by nephelometric method), Cl− 4 (by Mohr’s argentometric method), Ca2+ , Mg2+ (wersenian method) Na+ , K+ and total Fe (by atomic absorption spectrometry method). The following parameters were measured in the field: pH, water temperature, conductivity, dissolved oxygen and oxygen saturation. The remaining ones were measured in laboratory. Considering the wide gradient we used the canonical correspondence analysis (CCA, the method assuming unimodal relation of species and environment) for the investigation of relation of particular species to environment. Consequently, detrended correspondence analysis was applied for the description of ecological gradient size (beta-diversity)

Habitat requirements of Charetum intermediae phytocoenoses (ter Braak & Šmilauer 1998). Forward selection procedure was used to reduce number of environmental variables by means of Monte Carlo permutation test with 999 permutations. Variables were removed until the level of significance p < 0.05 was reached.

Table 1. Synoptic table of 20 phytosociological relevés of Charetum intermediae from the studied lakes of western Poland. Abundance Species

1. Phytosociological characteristic of the Charetum intermediae phytocoenoses in natural lakes of western Poland The associations of Charetum intermediae were recorded in 13 lakes; in 8 of them they created phytocenoses dominating the vegetation within the limits of the water surface. The patches were located mostly in central parts of the basins. Sometimes, in considerably shallowed lakes (max. up to 1 m deep), whose central parts were occupied by the phytocenoses with Nymphaea × borealis (cross-breed forms of Nymphaea alba s.s and Nymphaea candida), the charophyta meadows with Chara intermediae, in zone of vegetation, were situated on the peripheries. It was only in the Zamorze Lake where the Charetum intermediae appeared in a 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 phytolittoral. The analysed charophyta meadows were poor in species, single-layered and considerably dense (Table 1). For most cases Chara intermedia was created onespecies phytocenoses. Out of the 15 species recorded, only Utricularia vulgaris, Utricularia minor, Chara globularis and Chara delicatula reached the II degree of constancy. The vegetation plots dominated by Chara intermedia showed a wide spectrum of species ranging from characteristic for poor and rich waters, being a complex of transitions between moderate and hard aquatic environment. CCA analysis revealed 3 groups. In the canonical correspondence analysis all the variables explained 31% of the variation but not all the parameters were significant (p < 0.05) in Monte Carlo permutation test. The first group was floristically poor, single-species and connected with the deepest sites (1.5–3 m) located in central parts of the basins. The second group of phytocenoses with Chara intermedia appeared in configurations with other charophyta species, e.g. Chara tomentosa, C. globularis, Nitellopsis obtusa, or with such vascular plants as Stratiotes aloides, or Myriophyllum verticillatum. In this group, among the accompanying species it was Utricularia vulgaris which exhibited the greatest constancy. Finally, the third group of phytocenoses showed a characteristic presence of Chara delicatula and Utricularia minor. In patches of shallow water, less than 0.5 m deep, especially in the third group, some nympheids could be observed (Nymphaea alba and Nymphaea × borealis) or, sporadically, examples of swamp vegetation such as Typha angustifolia, Typha latifolia and Phragmites australis.

Constancy 5

Ch. Charetum intermediae Chara intermedia

Results

659

4 3 2 1 + r

16 4

.

.

.

.

.

V 100

Ch. Charetea fragilis: Chara globularis Chara delicatula Chara tomentosa Nitellopsis obtusa

. . . .

. . . .

. . . .

. 2 3 2 1 . . 1

4 . 1 .

. . . .

II II + r

30 25 10 5

Ch. Potametea: Nymphaea× borealis Nymphaea alba Myriophyllum verticillatum

. . .

. . .

. . .

. 2 1 1 . .

1 . 2

. . .

I + +

15 10 10

Accompanying species: Utricularia vulgaris Utricularia minor Stratiotes aloides Typha latifolia Phragmites australis Hydrocharis morsus-ranae Lemna minor Typha angustifolia

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

7 5 . 1 1 1 1 1

. . . . . . . .

II II I r r r r r

40 25 10 5 5 5 5 5

1 . 2 . . . . .

2. Physical and chemical properties of water in Charetum intermediate stands The charophyta meadows with Chara intermedia appeared in strongly shallowed lakes with the dominating habitat type based on substratum of calcium gyttjas, strongly hydrated, and with a high concentration of organic matter. The water depth of the Charetum intermediae phytocenoses was mostly 1 m; only in the Czarne Lake the patches present up to 3 m deep could be found. It has to be pointed out, however, that in most of the cases the charophytes grew up to the very water surface, and in some cases were even floating above the bottom without touching it. The habitats of Charatum intermediae phytocoenoses were characterized with respect 16 water properties. Ranges and mean rates were contained in Table 2. The charophyta meadows habitat is characteristic of high water colour and its humic nature, visible in a considerable concentration of DOC. Despite the high water colour indices, the transparency of water were reached to the bottom of the lakes. The content of humic substances in water was higher than that of most of the natural waters in the Wielkopolska region (Bara
lkiewicz & Siepak 1994). The pH of water ranged from slightly acidic to alkaline; in most cases, however, it was about neutral. From numeric data it might follow that the recorded phytocenoses were connected with meso- and eutrophic waters. They exhib− ited considerably high NH+ 4 and NO3 contents and an average degree of water mineralization. The content of analysed nitrogen forms varied widely. The waters + + were poor in PO3− 4 , Na , K , total Fe and, in most − of the phytocenoses, in Cl . The habitats of the Chara

M. G˛ abka

1.0

660

Axis 2 Ca EC

Phraus Nymalb

SO4 pH

SD

colour

depht

Lemmin O2 dissolved Utrvul Chaglo

P-PO4

K

Chaint Fe N-NH4

Na

Axis 1 Nitobt

Nymbor

Typlat DOC Stralo Myrver Utrmin Mg Chadel N-NO3

Chatom

Cl

-0.6

Typang Hydmor

-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 chemical properties (see Methods for details) of water found in habitats of Charetum intermediate. Property Depth of water SD Colour DOC pH O2 dissolved conductivity N-NH+ 4

Range

mg O2 L−1 µS cm−1 mg N L−1

0.15–3.00 0.15–2.00 6.00–86.00 5.30–26.46 6.80–7.80 3.94–12.20 176.00–556.00 0.04–0.58

1.01 0.91 36.85 13.21 7.31 7.41 402.55 0.22

N-NO− 3

mg N L−1

0.00–0.50

0.13

Total Fe Ca2+ Mg2+ Na+ K+ SO2− 4 Cl−

mg mg mg mg mg mg mg mg

0.00–0.20 0.00–0.12 24.51–102.11 2.17–26.04 1.03–16.32 0.23–5.20 0.00–140.00 4.00–70.00

0.08 0.04 47.78 7.74 4.78 1.03 34.50 11.7

P-PO3− 4

m m mg Pt L−1 mg C L−1

Mean

PO4 L−1 Fe L−1 Ca L−1 Mg L−1 Na L−1 K L−1 SO4 L−1 Cl L−1

n = 20 (only for DOC – dissolved organic carbon n = 18)

intermedia meadows were characteristic of high water oxygenation. The Charetum intermediae phytocoenoses showed a wide range of Ca2+ , Mg2+ and SO2− con4 tent. The content of Ca2+ was characteristic of soft and medium-hard waters. Smaller values of elements connected with the concentration of Ca2+ and Mg2+

in the habitats of charophyta meadows were recorded in lakes with strongly developed surrounding parts of transitional peat-bogs. Figure 2 presents the relationships between habitat variables and the species constituting the Chara intermedia charophyta meadows. Following stepwise selection (Monte Carlo permutation test) among 16 parameters, 5 quantitative environmental variables turned out to be significant: Ca2+ , Cl− , Mg2+ , colour of water and dissolved oxygen. In forward selection procedure the remaining variables explained 57% of variation in the species data. The first axis is to a large extent correlated with Cl− , Na+ and K+ . These were the patches with the participation of Chara tomentosa and Nitellopsis obtusa that developed best in waters rich in these elements. Worth noticing, too, is the distribution of most of the species along the other axis. We may conclude, then, that it is the presence of Ca2+ and SO2− 4 , together with conductivity, that seems to be decisive for the species configuration of the Charetum intermediae charophyta meadows. In the case of phytocenoses with habitats rich in Ca2+ , we could observe an additional participation of such species as Chara globularis, Utricularia vulgaris and Nymphaea alba. The waters of these species were also, to some extent, coloured and poor + in NO− 3 and NH4 . It was the presence of Utricularia minor and Chara delicatula in the patches of Charetum intermediae that served as an indicator of the habitats

Habitat requirements of Charetum intermediae phytocoenoses poor in Ca2+ . The patches with the presence of these species developed better in more highly coloured habi+ tats, richer in NO− 3 and NH4 . Discussion In shallow, marcophytes-dominated lakes, charophytes not only tend to occupy the habitats suitable for them, but they also influence their quality (van der Berg et al. 1999; van Donk & van Bund 2002). Particularly, they increase the transparency of water and lower its abundance in nutrients and calcium compounds, thus shaping the habitat conditions (Szefer 2001; Kufel & Kufel 2002). The relationship between the occurrence of charophytes and proper light and trophic conditions has been pointed out in a number of studies (e.g. Baszy´ nski & Karczmarz 1997; Blindow 1988, 1992; van der Berg et al. 1999). On the basis of habitat analyses of charophyta meadows dominated by Chara intermedia we may observe special relationships between the abiotic elements important for the ecology of the Characeae. The zone of transitional peat-bogs, often of a considerable area, surrounding most of the lakes was a source of allochtonic humic acids which exert a limiting influence on light conditions (e.g. Górniak 1996; Hutorowicz 2001), and thus prevent the charophytes from settling in the deepest parts of this type of lakes (more than 3m deep). Therefore, Charetum intermediae occurred in shallowwater conditions, overgrowing the water up to the water table. In deeper lakes, or on sites located in central parts of the basins, charophyta meadows were raised up to the water table. This position was connected with the physiological photosynthetic processes, as it provided the macroalgae with proper light conditions (G˛abka 2004). The presence of Charetum intermediae in shallow basins can be interpreted as an indication of waters rich in nutrients and humic acids, and classified sometimes as humotrophic waters. Taking into consideration the internal floristic and habitat diversity of charophyta meadows dominated by Chara intermedia, we can distinguish 2 groups of phytocenoses: (I) appeared on sites poor in Ca2+ and rich in nutrients, in contrast to the group (II), connected with hard waters, especially those + poorer in NO− 3 and NH4 . Both groups of phytocenoses were rich in DOC and developed in coloured waters. High content of nutrients found in well-lighted shallow habitats of Charetum intermediae can be related to the periodic dissociation of humic acids and the release of ammonium and phosphate ions into water (e.g. Koenings & Hooper 1976; Franco & Heath 1982; Jones et al. 1988; Wojciechowski 1990; Wojciechowski & Górniak 1990). It is believed that the process of photodegradation of the chelation connectionsof humic acids and minerals compounds, observable in hardwater basins, is one of the factors influencing their eutrophication (Jones et al. 1988; Wojciechowski 1990; Wetzel 1992). That is why the phytocenoses with Chara intermedia appeared in relatively eutrophic waters. On the other hand, the constant supply of humic sub-

661

stances flowing from the immediate catchment basin, is an important factor shaping habitat conditions of charophyta meadows with Chara intermedia. Factors connected with the concentration of Ca2+ have to be considered as the most important habitat parameters shaping the occurrence of the analysed charophyta meadows. Charetum intermediae appeared both in waters rich in calcium compounds (alkaline) and in those poorer in Ca2+ (with neutral reaction). It has to be pointed out that similar conclusions could be drawn from earlier studies of Charetum intermediae, less extensively documented with habitat data (Karczmarz & Malicki 1979; Krause 1981; Doll 1989). The appearance of this syntaxon was usually connected with hard waters rich in the Ca2+ compounds; less frequently was it related to mid-bog lakes poorer in Ca2+ . Chara intermedia grows primarily in shallowed lakes developed in the process of succession (D˛ambska 1966; Karczmarz & Malicki 1979; Krause 1981; G˛abka 2004). This study demonstrates that, in vegetation plots of the analysed meadow, it is the presence of the species Utricularia minor and Chara delicatula that may be interpreted as an indicator of habitats of charophyta meadow with small calcium content (with all its consequences). In contrast, in the case of waters rich in calcium, it may be the presence of Utricularia vulgaris, Chara globularis and Nymphaea alba. As far as the habitats of charophyta meadows with Chara intermedia are concerned, in the case of lakes with strongly developed zones of surrounding peatbogs, the content of factors related to the hardness of water was noticeably lower. We may suppose that, together with the development of peat-bogs, which serve as a biogeochemical barrier preventing the outflow of Ca2+ to the basin, the domination of Charetum intermediae in the lake may be an element responsible for the lowering of the hardness of water (G˛abka et al. 2004). It may result from the fact that the charophytes use calcium compounds dissolved in water as a constructive element of their thallus, and thus lower their concentration in water (Go
ldyn 1984; van der Berg et al. 1999; van der Berg et al. 2002). Therefore, charophyta meadows with Chara intermedia play a crucial role in the lowering of the hardness of water towards the soft water conditions They tend to appear in the habitats whose substrata are rich in calcium (G˛abka 2004; G˛abka et al. 2004), but whose concentration of calcium in the water is considerably lower. Charophytes are said to limit the development of phytoplancton, not only because of the competition for nutrients, but also because their allelophatic impact (e.g. van Donk & van de Bund, 2002). This observation would imply the theory of alternative stable states and a number of intermediate unstable ones (Scheffer 1989, 1990, 2001; Scheffer et al. 1993; Scheffer & Jeppesen 1998). And indeed, this observation may be confirmed by the analysis of the chlorophyll content in the phytoplancton of the analysed lakes. As both the qualitative and the quantitative analyses of plancton algas coming from the habitats with Chara interme-

662 dia demonstrated, in most of the cases we find a poor, mesotrophic character of the phytoplancton, despite the habitats abounding in nutrients, resembling clear water ones (G˛abka & Owsianny 2005). However, in some cases we could find a considerable biomass of phytoplancton, despite the fact that C. intermedia occupied almost the entire bottom of the analysed lakes. These examples might illustrate different variants of unstable states. Yet, in all of the lakes only a small participation of Cyanobacteria in phytoplancton could be detected. This fact may confirm the alleged allelophatic effect of charophytes because their inhibiting impact was most commonly noticed in the case of this particular group of algae (Berger & Schagerl 2004). Therefore, we may conclude that the presence of Charetum intermediae in very shallow, developed in the process of succession lakes of the Wielkopolska region, is a resultant of two factors: firstly, of light conditions, related to the concentration of humic substances and the possibility for charophyta meadows to grow up to the water table, and secondly, of the concentration of elements related to the hardness of water. References Bara
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