Jolanta EJSMONT-KARABIN 1 *, Andrzej HUTOROWICZ 2

POLISH JOURNAL OF ECOLOGY (Pol. J. Ecol.) 59 3 569 576 2011 Regular research paper Jolanta EJSMONT-KARABIN 1 *, Andrzej HUTOROWICZ 2 1 Department of Hydrobiology, Institute of Biology, University of Białystok, Świerkowa 20 B, 15-950 Białystok, Poland, *e-mail: jolanta@onet.pl (corresponding author) 2 The Stanisław Sakowicz Inland Fisheries Institute, Oczapowskiego 10, 10-719 Olsztyn-Kortowo, Poland, e-mail: ahut@infish.com.pl ROTIFERA COMMUNITIES ASSOCIATED WITH INVASIVE VALLISNERIA SPIRALIS L. (HYDROCHARITACEAE) VERSUS NATIVE MACROPHYTES IN THE LAKES HEATED BY POWER STATIONS (KONIN LAKES, W. POLAND) ABSTRACT: The role that invasive Vallisneria spiralis L. plays in determining the species richness of the rotifer community was examined in the littoral zone of two heated (by power stations) lakes near Konin (W. Poland) (Lake Licheńskie area 153.6 ha, max. depth 13.3 m and Lake Ślesińskie area 148.1 ha, max. depth 25.7 m). Vallisneria spiralis is a thermophilic and vegetative reproducing species which has been recorded in the lakes since the 1990s. It spreads very quickly in the lakes, forming monospecific, dense beds which, force out all other submerged vegetation. Samples were collected in August 2004 on 8 littoral stations of Lake Licheńskie and Ślesińskie. Five-liter samples of water (plankton species) and macrophytes (epiphytic species) were elaborated separately. An analysis of the taxonomic structure of rotifer communities inhabiting single-species Vallisneria beds and mixed-species (Vallisneria plus other macrophyte species) beds showed that both communities were relatively rich in species and similar in terms of species composition. A total of 100 species of Monogononta were identified. Single-species Vallisneria beds were inhabited by 77 species, whereas 82 species were found at stations with mixed vegetation. Species diversity was relatively high in both types of macrophyte assemblages. Numbers of rotifer species inhabiting the single-species Vallisneria beds are among the average values observed in a littoral zone rich in macrophyte species from lakes of different morphometry and trophic state. The above observations confirm part of the conclusions from literature that invasions by new plant species do not always lead to a decline in the habitat value for native animals. Otherwise, the invaded plant creates the habitat easily colonized by the native plankton and epiphytic invertebrates. KEY WORDS: Vallisneria spiralis, Rotifera, lake, littoral, macrophyte invasion 1. INTRODUCTION Invasive species can seriously alter a habitat, especially if they are the key species of a community (Kelly and Hawes 2005). Epiphytic macroinvertebrate communities may be indirectly altered through the replacement of native macrophytes by exotic ones, even if the macrophytes are of the same genus (i.e. Myriophyllum) and similar morphology (Wilson and Ricciardi 2009). Vallisneria spiralis (Hydrocharitaceae) is an exotic, tropical hydrophyte. In the last twelve years it has colonized three lakes in the vicinity of Konin (Kujawskie Lake District, Western Poland) (Hutorowicz et al. 2006). The lakes are included in the open cooling system of heat and power stations. Environmental conditions and biota, the effect of water heating on journal 27.indb 569 2011-10-06 10:09:15

570 Jolanta Ejsmont-Karabin and Andrzej Hutorowicz the physico-chemical properties of the water, primary and secondary production, species composition and densities of plankton have been the subject of long-term studies (Hillbricht-Ilkowska et al. 1988, Simm 1988, Z danowski 1994, Z danowski et al. 2002). The high temperature of the water in the lakes was one of the most important reasons for the rapid invasion the littoral zone of the lakes by Vallisneria spiralis (Hutorowicz 2006). In Lake Licheńskie Vallisneria formed very dense single-species phytocoenoses and almost entirely displaced native submerged macrophytes. In Lake Ślesińskie, the invader formed smaller phytocoenoses of the Potamo perfoliati-vallisnerietum spiralis association, and was accompanied by non-dominants like Myriophyllum spicatum, Ceratophyllum demersum, Najas marina and Batrachium circinatum (Hutorowicz et al. 2006). The composition and abundance of rotifer communities in the littoral zone of lakes is greatly influenced by the species of macrophyte (Kuczyńska-Kippen 2000, Duggan et al. 2001). Experimental studies (Reed 1978) have shown that physical complexity increases diversity in unfertilized microecosystems. The change from the former mixedspecies macrophyte associations into singlespecies ones due to the invasion by Vallisneria spiralis might decrease diversity of the rotifer communities inhabiting the littoral zone of the studied lakes. The aim of the study was to test the above hypothesis by comparing rotifer communities inhabiting mixed-species beds (i.e. composed by Vallisneria and other macrophyte species) and single-species Vallisneria beds. 2. METHODS Samples were collected during a single survey (August 2004) on 8 littoral stations (Table 1) of Lake Licheńskie and Lake Ślesińskie. Plankton and epiphyton were sampled and prepared separately. Ten liter samples of water with macrophytes were collected from the centers of macrophyte beds, then ten macrophyte leaves were cut and gently pulled out. Epiphytic rotifers were removed from live macrophytes using a soft bristle brush. Epiphytic rotifers were condensed on a plankton net which had a mesh size of 30- mm, transferred into bottles and fixed with Lugol s solution and then with 4% formalin. The plant material devoid of epiphyton was dried overnight at 60 o C and weighed. Fiveliter samples of plankton material were condensed on a plankton net which had a meshsize of 30-mm and fixed with Lugol s solution and then with 4% formalin. All rotifers were counted and identified, in three subsamples each equal to 10% of the sample, under the light microscope Nikon Eclipse E600 at 400 Table 1. Characteristics of the sampling stations. Date Station Temp. ( o C) Description 16.08. Licheń 1 At a bay near the village Stary Licheń; large area overgrown with 28.0 (SNG1) single-species Vallisneria phytocoenose 18.08. Licheń 2 At the eastern shore of Lake Licheńskie; single-species Vallisneria phytocoenose 26.8 (SNG2) Licheń 3 At the western shore of Lake Licheńskie; single-species Vallisneria phytocoenose (SNG3); phytocoenose composed of Myrio- (SNG3) 17.08. 25.9 (MIX3) phyllum spicatum 90% and Vallisneria 10% (MIX3) 17.08. Channel Outlet of the channel supplying warm water to Lake Wąsowsko- 28.4 (SNG4) Mikorzyńskie; single-species Vallisneria phytocoenose 16.08. 16.08. 16.08. Licheń 4 (MIX1) Licheń 5 (MIX2) Ślesin (MIX4) 27.7 26.7 25.2 Near the village Wygoda; a shore with a belt of reed; phytocoenose of submerged macrophytes composed of Vallisneria (90%) and Najas marina (10%) Western shore of southern part of Lake Licheńskie; mixed phytocoenose of submerged plants with domination of Vallisneria (ca. 70%) and Potamogeton nodosus (ca. 30%) At a shallow bay at the western shore of Lake Ślesińskie; mixed phytocoenose of submerged plants with domination of Vallisneria (ca. 65%) and Ceratophyllum demersum (ca. 15%), Myriophyllum spicatum (15%) and Batrachium circinatum (ca.5%); journal 27.indb 570 2011-10-06 10:09:15

Invasive Vallisneria impact on littoral Rotifera 571 and 100 magnification. The numbers of plankton rotifers were expressed as individuals per liter and those of epiphytic as individuals per gram of dry weight of plant biomass. The index of percentage similarity of community (PSC) (Whittaker and Fairbanks 1958) was used: PSC = 100 0.5 (a b) = min. (a, b) (1) where a and b are percentages of individuals of each species in the total numbers of the communities of lakes A and B, compared in pairs. Statistical analyses were run with STA- TISTICA (Statsoft. Inc.) software. Probability levels of 0.05 were considered significant. Data were examined by t-tests. All proportion data were arcsin-square-root transformed prior to statistical analyses. 3. RESULTS An analysis of the taxonomic composition of rotifer communities inhabiting singlespecies Vallisneria beds and mixed-species Vallisneria beds showed that both habitats were relatively rich in species. A total of 100 species of Monogononta were identified. Single-species Vallisneria beds were inhabited by 77 species and the mean for the stations was 43 ± 6 (from 36 to 51). The slightly higher figure of 82 species were found at stations with mixed vegetation. The mean for the mixed vegetation stations was 45 ± 11 (from 34 to 59). A comparison of the communities occupying the two types of habitats, i.e. plankton and epiphyton, showed that the differences between rotifer densities and taxonomic composition in single-species and mixedspecies macrophyte assemblages are weak or did not exist. Although the density of planktonic monogononts from the mixed-species macrophytes was nearly twice (387 ± 380 ind. l 1 ) that recorded from the single-species Vallisneria beds (166 ± 72 ind. l 1 ), the differences were not significant statistically (P = 0.30). The higher mean density in the mixed-species macrophyte stands, resulted from the extremely high values at one station, i.e. MIX1 (Table 2). Densities of epiphytic monogononts were similar in both types of aquatic vegetation with mean values of 1754 ± 1234 ind. l 1 in Vallisneria and 1997±1070 ind. l 1 in mixed assemblages. Slightly fewer species occurred among Vallisneria (24 ± 4), than among mixed-species vegetation (28 ± 4), however, the difference was Table 2. Quantitative and qualitative characteristics of monogonont communities inhabiting singlespecies and mixed assemblages of macrophytes in the Konin lakes in summer 2004. Stations see Table 1. SNG1 SNG2 SNG3 SNG4 MIX1 MIX2 MIX3 MIX4 Parameters Vallisneria beds Mixed-species beds Plankton Density (ind. l 1 ) 256 193 109 106 948 255 237 108 Number of species 28 27 21 19 27 23 29 33 Shannon s index of diversity 3.07 3.06 3.69 3.65 1.34 2.24 3.67 3.40 Epiphyton Density (ind. g DW 1 ) * 1097 3517 743 1657 1290 3582 1421 1694 Number of species 15 36 30 42 30 29 19 46 Shannon s index of 1.42 4.05 2.86 3.71 3.33 2.56 3.42 4.50 diversity * individuals per gram of dry weight of the plant biomass journal 27.indb 571 2011-10-06 10:09:15

572 Jolanta Ejsmont-Karabin and Andrzej Hutorowicz Stations Table 1 Fig. 1. Comparison of the percent contribution of dominant species to the total numbers of plankton communities of Rotifera from single-species and mixed-species macrophyte beds. Stations see Table 1. Stations Table 1 Fig. 2. Comparison of the percent contribution of rotifer dominants to the total numbers (ind. g macrophyte DW 1 ) of their epiphyton communities inhabiting single-species and mixed species macrophyte beds. Stations see Table 1. not significant (P = 0.21). Communities of epiphyton were composed of an identical number of species (31 ± 11) in both types of macrophyte cover. The Shannon-Wiener s diversity of Rotifera was relatively high in all types of habitats and averaged 3.37 ± 0.30 for plankton in the single-species macrophyte beds and 2.66 ± 1.08 for the mixed-species vegetation. The diversity journal 27.indb 572 2011-10-06 10:09:15

Invasive Vallisneria impact on littoral Rotifera 573 of epiphyton rotifer communities was 3.01 ± 1.17 and 3.45 ± 0.80, respectively (Table 2). Significant differences, however, may be seen in the structure of the littoral plankton species (Fig. 1). Three stations were dominated by a pelagic rotifer Polyarthra remata Skorikov, and there were two stations with the mixed-species macrophyte beds and one station with a single-species Vallisneria stand. Domination of the species was characteristic for the most numerous rotifer communities. The taxonomic composition of communities inhabiting both single- and mixed-species macrophyte assemblages at station Licheń 3 (SNG3 and MIX3) was less diversified than in all the remaining communities (Fig. 1). An analysis of the percentage similarity of the community (PSC) for monogonont plankton communities indicated a higher similarity of rotifers from single-species beds. The mean value of the index calculated for all the possible pairs of stations was 43% (SD = 5%), and it ranged from 37 to 51%. Hence, even in the case of rotifers from single-species beds, less than half of the community was similar in the two compared stations. Markedly higher differences in species composition of Rotifera were noted for communities occupying mixed-species assemblages of macrophytes. The mean value of the PSC index was as low as 35.3% (SD = 24.3), but certain values ranged widely, from 5.9 to 62.7%. However, if station 3 is omitted, the PSC for the remaining communities becomes higher than in single-species beds and accounts for 56.5% (SD = 6.4). In comparison to littoral plankton, epiphytic communities of Rotifera were less differentiated both in single-species Vallisneria beds and mixed-species ones (Fig. 2). However, epiphytic monogononts from vegetation of mixed-species seem to be more abundant. All communities consisted of similar dominants, with a few exceptions like colonial Lacinularia flosculosa (Müller) dominating at station MIX2 in Lake Licheńskie (with macrophytes dominated by Potamogeton sp.). As regards epiphyton in single-species Vallisneria, PSC analysis for monogononts indicates a lower similarity of the rotifer communities than that of the plankton communities. The mean value of the index for all pairs of the stations accounted for 37.0% (SD=14.8), and their values ranged from 14.8 to 51.5%. Thus, also in the case of epiphytic Rotifera from single-species Vallisneria beds, less than half of the communities were taxonomically identical in compared pairs of stations. Epiphytic communities of Rotifera from mixed-species macrophyte stands were extremely differentiated. The mean PSC value accounted for only 20.0% (SD = 19.3), and the values range was very wide, from 7.8 to 57.5%. The lowest PSC values were found for pairs of communities from particular stations with the rotifer community from the stations MIX3. Comparison of the species composition of the plankton and epiphytic monogonont communities at the same stations indicated significant differences between the commu- Fig. 3. Mean percentage of Bdelloidea in densities of planktonic and epiphytic communities of Rotifera inhabiting single-species and mixed-species macrophyte beds (SD standard deviation; SE standard error). journal 27.indb 573 2011-10-06 10:09:17

574 Jolanta Ejsmont-Karabin and Andrzej Hutorowicz Fig. 4. Numbers of rotifer species in macrophyte beds from different lakes in northeastern Poland and their relation to the number of analyzed samples. Black circle shows number of species found in the mixed-species macrophyte beds; the dashed one in single-species Vallisneria beds in the studied Konin Lakes; open circles data for the remaining lakes. nities as well as their strong attachment with the occupied habitats. The mean value of the Index of Percentage Similarity for pairs of communities inhabiting open waters and epiphyton was ca. 23% in both single-species and mixed-species beds. The relatively high range of PSC values, from 6 to 58%, may be the result of the mechanical influence of waves causing detachment of the epiphyton. Bdelloids were another group playing an important role in the rotifer communities. They were less abundant in waters surrounding macrophytes, but they decidedly dominated in epiphyton at most of the stations (Fig. 3). The presence of bdelloids can be easily spotted as these animals usually creep, and only sometimes swim. Their contribution to the total density of Rotifera did not differ in single-species and mixed-species beds as regards both plankton and epiphyton communities. 4. DISCUSSION Rotifer communities inhabiting Vallisneria stands seem to be relatively rich in species, although a rotifer habitat built with one macrophyte species of rather simple architecture is not expected to offer very many niches. The view that there are relatively rich rotifer communities inhabiting Vallisneria beds may be verified by the results of a comparison of the number of rotifer species in Vallisneria beds and data from littoral vegetation of different lakes (Fig. 4). The number of rotifer species inhabiting the uniform sites of Vallisneria are among the average values (or even slightly exceeding them) observed in the littoral zone rich in macrophyte species from lakes of a different morphometry and trophic state. Invasion by macrophytes can cause significant shifts in lake productivity, species composition and food web dynamics as it has been shown in Lake Wanaka (New Zealand) (Kelly and Hawes 2005). The lake was partly invaded by Lagarosiphon major and Elodea canadensis, which formed dense plant beds. Benthic invertebrate communities were less dense and less diverse in native than in exotic plant beds. On the other hand, studies on macroalgal invasions showed different response from epiflora and epifauna to changes in their environment. The invasions of Fucus evanescens (brown alga of arctic origin) of European coasts had rather a low direct effect on the biodiversity of epiphytic communities associated with Fucus evanescens (Wikstrom and Kautsky 2004). According to the authors, similarity of the epiphytic community for two species of Fucus suggests that most epiphytic species show low host specificity. On the other hand, the introduced Caulerpa taxifolia had fewer species of associated invertebrates than native algae (B ellan-santini et al. 1996). Laboratory experiments were conducted by Weis and Weis (2000) on the behavior- journal 27.indb 574 2011-10-06 10:09:17

Invasive Vallisneria impact on littoral Rotifera 575 al response of three species of native estuarine animals to invasive Phragmites australis. Their experiments showed that invasions by new plant species do not always lead to a decline in habitat value for native animals. This conclusion may be confirmed by the results concerning the Sargassum muticum invasion of the Atlantic coast side of Spain (Viejo 1999). The invasive species had an associated fauna very similar to that of the native seaweeds. Experimental studies conducted by Theel et al. (2008) in the field (pond) and the experimental treatments showed that macroinvertebrate abundance, richness, and biomass in a hydrilla-dominated habitat did not differ significantly from a diverse plant habitat. Nevertheless, the authors suggest that a shift from a natural mosaic of vegetated habitat to a highly complex monotypic habitat may reduce spatial heterogeneity and influence macroinvertebrate assemblages. Disturbed or cultivated habitats are recognized as especially vulnerable to invasion (Elton 1958). The Konin lakes have undergone large-scale habitat disturbances. This is due to the fact that, since 1958 the lakes have been part of the open cooling system of the Konin Heat and Power Station. Warm waters supplied to Lake Licheńskie all year round and to Lake Ślesińskie in the summer markedly increase the temperature of the water of the lakes (up to 25.2 o C in Lake Ślesińskie and 28.0 o C in Lake Licheńskie). Such disturbances promote the invasions of aliens (Heywood 1989). This may explain the very fast colonization of the littoral zone by Vallisneria spiralis. Higher temperatures may also promote invasions by exotic rotifers associated with the exotic plants. Such co-invasions of insects visiting exotic flowers were already observed in temperate forests of the southern Andes (Morales and Aizen 2002). Without this disturbance effect, colonization of Vallisneria created sites by new species of Rotifera would be unsuccessful. Shurin (2000) has done experiments on colonization of fishless ponds by zooplankton. He has shown that zooplankton communities are nearly saturated with species and that biotic interactions exclude many potential invaders. Change in habitat caused by an increase in water temperature may weaken the native populations defense against invaders. However, the high diversity of rotifers living amongst Vallisneria originates mainly from the high number of native species, as not very many exotic species of Rotifera were described from the site (Ejsmont-Karabin 2011). The new, exotic species did not play significant role in the biocoenose. Another explanation of the high species diversity may be because of the very simple architecture of the Valisneria leaves. These long, flat and relatively large macrophytes are easy to colonize but devoid of refuges. Thus rotifers living on and among them may be easily attacked by all types of predators. Cupelopagis vorax (Leidy), which occurred in the studied sites in comparatively large densities (Ejsmont- Karabin 2011), is a good example. This large rotifer is the kind of predator that needs such a flat area to sit and wait for its prey, i.e. ciliates and small rotifers (B evington et al. 1995). Macrophytes of such a simple architecture are also susceptible to destruction of their epiphytic algae by wave action. This can be seen by the presence of high densities of sessile rotifers in plankton samples. Thus, Vallisneria habitat may permanently be in the first stages of colonization, giving many species a chance to start building their populations. ACKNOWLEDGEMENTS: The study was financially supported by the Polish Ministry of Science and Higher Education grant no. 2 PO4G 088 26 5. REFERENCES Bellan-Santini D., Arnaud P.M., Bellan G., Verlaque M. 1996 - The influence of the introduced tropical alga Caulerpa taxifolia, on the biodiversity of the Mediterranean marine biota J. Mar. Biol. Assoc. UK 76: 235 237. Bevington D.J., White C., Wallace R.J. 1995 Predatory behavior of Cupelopagis vorax (Rotifera; Collothecacea; Atrochidae) on protozoan prey Hydrobiologia, 313 314: 213 217. Duggan I.C., Green J.D., Thompson K., Shiel R.J. 2001 The influence of macrophytes on the spatial distribution of littoral rotifers Freshw. Biol. 46: 777 786. Ejsmont-Karabin J. 2011 Does invasion of Vallisneria spiralis L. promote appearance of rare and new rotifer (Rotifera) species in littoral of the lakes heated by power station (Konin lakes, W. Poland) Pol. J. Ecol. 1: 59: 201 207. journal 27.indb 575 2011-10-06 10:09:17

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