Jolanta EJSMONT-KARABIN

POLISH JOURNAL OF ECOLOGY (Pol. J. Ecol.) 59 1 201 207 2011 Short research contribution Jolanta EJSMONT-KARABIN Department of Hydrobiology, Institute of Biology, University of Białystok, Świerkowa 20 B, 15-950 Białystok, Poland, e-mail: jolanta@onet.pl 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)? ABSTRACT: Large-scale human-caused ecosystem disturbances may create new habitats. A good example may be long-lasting disturbances in five lakes (area from 148 to 379 ha, max. depth from 3 to 38 m) integrated into the cooling system of the power plants near Konin (52 17.8 52 23.3N, 18 14.4 18 20.7 E, West Poland). In the middle of the 1990s Vallisneria spiralis began to colonize littoral zone of three of lakes and in 2002 it appeared also in fourth one. This species formed dense patches and almost completely displaced other submerged macrophytes. An aim of the study was to test a hypothesis that the appearance of rare and new for Polish fauna rotifer species might be a result of changes in littoral habitats of these lakes particularly caused by the invasion by Vallisneria spiralis. Studies were carried out in the years 2004 2006 on 3 6 littoral stations in each lake. Five-liter samples of water with macrophytes were collected from a center of macrophyte beds. Plankton (free-swimming) and epiphytic (connected with macrophyte surface) samples were elaborated separately. As many as 167 monogonont species were recorded during the three-years studies. From among them 6 species were new in Polish fauna. These were: Asplanchnopus hyalinus Harring, Beauchampia crucigera (Dutrochet). Lecane inopinata Harring & Myers, Lecane shieli Segers et Sanoamuang, Lecane undulata Hauer and Lepadella apsida Harring. The species are eurythermic or warm-stenothermic. Species new to the rotifer fauna of Poland were not numerous as they usually constituted less than 2% of the total density of rotifers. Thus, although the hypothesis that rare and new for Polish fauna rotifer species may appear in the littoral habitats of the heated Konin lakes was confirmed, it was also clear that the colonization of the habitats by rotifer invaders did not lead to their domination in the rotifer communities. KEY WORDS: Rotifera, Poland, heated lakes, Konin lakes, Vallisneria, invasive macrophyte Human-caused changes in the natural ecosystems may create new habitats as well as patches within the habitats. Such large-scale habitat disturbances may promote the invasion and spread of alien (not-indigenous) species (Elton 1958, Morales and Aizen 2002). An example are long-lasting disturbances in five lakes (area from 148 to 379 ha, max. depth from 3 to 38 m) integrated into the cooling system of the power plants near Konin (West Poland). The lakes were included into the system in two steps, i.e. when power plant Konin began to function and then power plant Pątnów (Hillbricht-Ilkowska and Z danowski 1988). As a result the significant changes were observed in water

202 Jolanta Ejsmont-Karabin Table 1. Frequency (in 97 samples) and maximum numbers of most frequent and new to Polish fauna rotifier species met amongst Vallisneria (plankton-free swimming species) and on macrophytes (epiphyton) in the years 2004 2006. Species Frequency % Plankton Maximum numbers (ind. l 1 ) Frequency % Epiphyton Maximum numbers (ind. g 1 DW) Free-living Lecane hamata (Stokes) 94 2691 75 3600 Euchlanis dilatata Ehrenberg 91 96 48 628 Lecane closterocerca (Schmarda) 91 248 94 2709 Lepadella patella (Muller) 91 3407 79 1710 Brachionus quadridentatus Hermann 88 171 56 748 Keratella cochlearis (Gosse) 82 469 14 129 Trichocerca elongata (Gosse) 82 116 46 68 Lecane bulla (Gosse) 79 988 65 2169 Lecane luna (Muller) 79 296 60 1258 Testudinella patina (Hermann) 71 911 63 1465 Lecane aculeata (Jakubski) 65 1297 41 1205 Colurella uncinata (Muller) 62 62 32 241 Lepadella acuminata (Ehrenberg) 62 34 49 910 Polyarthra remata Skorikov 56 742 8 144 Polyarthra vulgaris Carlin 56 116 Pompholyx sulcata Hudson 53 123 5 24 Trichocerca porcellus (Gosse) 50 148 48 2106 Sessile Limnias ceratophylli Schrank 56 1210 46 4877 Ptygura furcillata (Krllicott) 26 14 52 140 Rare and new in Polish fauna Cupelopagis vorax (Lidy) 59 420 62 3700 Lecane shieli Segers & Sanoamuang 35 25 27 568 Asplanchnopus hyalinus Harring 9 20 2 7 Lepadella apsida Harring 3 1 5 40 Trichocerca mus Hauer 3 1 Lecane inopinata Harring & Myers 2 68 Lecane undulata Hauer 2 52 Beauchampia crucigera Dutrochet 2 11 temperature and through-flow. Environmental conditions and biota, effect of water heating on the physico-chemical properties of the water, primary and secondary production, species composition and densities of plankton communities were a subject of long-term and diverse studies (Hillbricht-Ilkowska et al. 1988, Simm 1988, Z danowski 1994, Zdanowski et al. 2002). It was shown that temperature of the lake waters increased considerably, up to maximum values of 30.9 C in shallow lake Lake Licheńskie and 27.7 C in deeper lake Lake Ślesińskie in the summer 1995 2000 (S ocha and Z danowski 2001). Vallisneria spiralis appeared in Konin lakes probably in the first half of the 1990s (Hutorowicz 2006). In the years 2002 2003 the species formed almost exclusively single-species beds in Lake Licheńskie (area of 153.6 ha, max. depth 13.3 m) and phytocoenoses composed of Vallisneria and Potamogeton perfoliatus L., Myriophyllum spicatum L. and other macrophyte species in Lake Ślesińskie (area 148.1 ha, max. depth 25.7 m) (Hutorowicz 2006). The introduction of alien aquatic plants into littoral zone may alter the complex web of biotic and abiotic interactions. The reduction

Vallisneria invasion and appearance of new rotifer species 203 of the habitat complexity may lead to reduction of macroinvertebrate diversity (Krull 1970, Ke ast 1984). Thus, also microinvertebrates (e.g. rotifers) may probably response in similar way to colonization of L. Licheńskie and L. Ślesińskie lakes by Vallisneria spiralis. Introduction of new species of macrophytes usually has significant influence on animal comunities (Posey 1988, Talley and Levin 2001) and may result in co-invasion of new species of invertebrates. Although it has been found that native biotic interactions exclude many potential invaders (Shurin 2000), Vallisneria occupying large areas (i.e. creating single-species phytocoenoses occupying the bottom to a depth of 2.5 m) of a near-shore zone creates new littoral habitat, which can help invading species to compete successfully with native communities. As two studied lakes are artificially heated and warm water is supplied to the Lake Licheńskie all year round, littoral communities of Rotifera may be enriched with exotic warm-stenothermic species. Morales and Aizen (2002) have shown that alien plant (exotic flowers) species could facilitate the invasions of some exotic flower visitors to disturbed habitats. An aim of the study was to test a hypothesis that the appearance of rare and new for Polish fauna rotifer species may be a result of changes in the littoral habitats of Konin lakes through heating lake waters and invasion of Vallisneria spiralis. Samples were collected: in July 2004 on 8 littoral stations of Lake Licheńskie; 4 stations with single-species Vallisneria beds and 4 stations with mix-species beds (Ejsmont-Karabin and Hutorowicz, in press); in 2005, monthly from April till October in Lake Licheńskie and from August till October in Lake Ślesińskie. Six stations with single-species Vallisneria beds were studied in the former and three stations in the latter lake. in August 2006 on 14 stations (7 stations in 2 locations covered with exclusively Vallisneria beds) in Lake Licheńskie. Five-litre samples of water were taken from the middle of macrophyte beds, filtered through a plankton net of 30- m mesh size and fixed with 2% formalin. Samples of epiphyton (= rotifers living on the surface of macrophytes) were taken concurrently to plankton samples. Epiphytic rotifers were removed from macrophytes using a soft bristle brush, condensed on a plankton net of 30- m mesh size, transferred into bottles and fixed. The plant material devoid of epiphyton was dried overnight at 60 C and weighed. In total 97 samples were elaborated. The concurrently taken qualitative sample was analysed alive. Some of species considered as rare or new for fauna of Poland were described and photographed using a NIKON E600 microscope and the system of computer image analysis (LUCIA). An analysis of taxonomic structure of rotifer communities inhabiting Vallisneria assemblages showed that the communities were relatively rich in species if compared to littoral communities of some lakes in the Masurian Lakeland ( like Lake Kuc, Lake Łuknajno and Lake Mikołajskie) (Mu i r- head et al. 2006). As many as 169 monogonont species were recorded during the three-years studies. Although littoral plankton may be enriched in pelagic species, the community was consistedwith markedly less rotifer species (115) than epiphyton (144). The most common genera were Lecane (with 24 species), Trichocerca (with 20 species) and Cephalodella (with 16 species). 44 species (26%) were encountered only once. As many as 42 species occurred in more than 20% of both plankton and epiphyton samples and from among them 19 species were found in more than 50% of plankton samples (Table 1). The most frequent and abundant species were: Lecane closterocerca (Schmarda), Lepadella patella (Müller), Lecane hamata (Stokes), Lecane bulla (Gosse), Brachionus quadridentatus Hermann, Lecane luna (Müller) and Testudinella patina (Hermann), Euchlanis dilatata Ehrenberg, Cupelopagis vorax (Leidy). Most of them are very common in Polish fauna, with an exception of Cupelopagis vorax, which was found only twice, by Czapik (1958) in the vicinity of Cracow and by Ejsmont-Karabin in the littoral of the River Biebrza ( East Poland ) (unpubl. data). This large (1 mm max. length) (Photo 1) and predatory species created very dense populations in Vallisneria beds reaching up to 3700 ind. g d. wt 1 of the macrophyte (Table 1).

204 Jolanta Ejsmont-Karabin Photo 1. Cupelopagis vorax, an alive female Photo 4. Lecane undulata, contracted Photo 2. Beauchampia crucigera, a contracted female out of its tube Photo 5. Lepadella apsida, contracted Photo 3. Lecane shieli, contracted Photo 6. Trichocerca mus, contracted

Vallisneria invasion and appearance of new rotifer species 205 Among rotifers found on and close to Vallisneria as many as 6 species seem to be new in Polish fauna. These are: 1. Asplanchnopus hyalinus Harring large i.e. ca 400 μm long animal with long and telescopically jointed foot; oviparous, predatory, cosmopolitan (Jose De Paggi 2002); during the present study females of the species were found in August both in epiphyton (7 ind. g d.wt 1 ) and in littoral plankton (5 to 20 ind. l 1 ) (Table 1); 2. Beauchampia crucigera (Dutrochet) large (up to 500 μm long), sessile rotifer with a characteristic very long dorsal antenna (Pennak 1978) (Photo 2); cosmopolitan (S egers 2007). It was found only once, in June 2005 on Vallisneria in a warm-water canal between lakes (Table 1). 3. Lecane inopinata Harring & Myers small, loricate rotifers with head aperture margins straight with angulate corners; characteristic feature are toes fused over proximal 1/3 and short, separated claws; warm-stenothermic and cosmopolitan species (S egers 1995). Its individuals were found in September 2005 on Vallisneria in a warm-water canal connecting two lakes (Table 1). 4. Lecane shieli Segers & Sanoamuang the species described in 1994 from one locality in Thailand (S egers and Sanoamuang 1994); females found in the Konin lakes were almost identical with those described from Thailand, i.e. their lorica was soft and irregularly folded (Photo 3), head aperture margins coincident and straight with sharp and straight spines in antero-lateral corners, toes long, parallel-sided and with weakly curved claws. The species occurred in relatively high numbers (up to 568 ind. g d. wt 1 of Vallisneria) at all studied stations, exclusively in August. 5. Lecane undulata Hauer small loricate rotifer, which resembles L. inopinata, but differs from the latter by toes fused only basally (Segers 1995) (Photo 4). Females of the species were found in August 2005 on Vallisneria in a warm-water canal. 6. Lepadella apsida Harring rare but cosmopolitan species, found previously in Senegal and Burundi (Baribwegure and Segers 2001). The species (Photo 5) occurred in summer on Vallisneria in Lake Licheńskie and the warm-water canal. Its highest density reached 40 ind. g d.wt 1 of the macrophyte. Besides Cupelopagis vorax, there was another species considered to be rare in Polish fauna of Rotifera, i.e. Trichocerca mus Hauer (Photo 6). Although the distribution of the species is poorly known (S egers 2003), some records (e.g. De Ridder 1985) indicate that the species is thermophilic. In Poland T. mus was recorded previously only once, by R adwan (1971), in pelagic waters of Lake Sumin (Łęczyńsko-Włodawskie Lake District, East Poland). A few individuals were found among Vallisnera in the littoral zone of Lake Ślesińskie. Species new to the rotifer fauna of Poland did not play an important role in the studied habitats. They occurred in 34% of the sampling points in epiphyton and 39% in the plankton occurring between the plants. Their contribution to the total monogonont rotifer density did not exceed 53% in epiphyton and 2% in plankton. However, even in epiphyton they usually constituted less than 2% of the total density. The species were present exclusively at stations covered with single-species Vallisneria beds and no one specimen belonging to this group of Rotifera was found in mix-species macrophyte assemblages (Ejsmont-Karabin and Hutorowicz, in press). Results of the studies conducted in the heated Konin lakes suggest that co-invasion of new sites by exotic species of Rotifera has taken place. Disturbed habitats are recognized as especially vulnerable to invasion (Elton 1958, Heywood 1989). There are many factors promoting such invasion in the studied habitats, all of them producing disturbances in rotifer habitats at different scales: an increase in temperature of the lake waters up to 25.2 C in the Lake Ślesińskie and 28.0 C in the Lake Licheńskie due to warm waters supplies to the Lake Licheńskie all year round and to the Lake Ślesińskie in summer.

206 Jolanta Ejsmont-Karabin very fast colonization of the littoral zone by single-species beds of the exotic Vallisneria spiralis. high susceptibility of Vallisneria to damages due to grazing by macroinvertebrates and fish (Li et al. 2010) and wave action. The latter is evidenced by a presence of high densities of sessile rotifers in plankton samples (Table 1). The effect of high temperature is evidenced by the above mentioned appearance of new for Polish fauna and warm-stenothermic species, like Lecane inopinata, L. shieli and Lepadella apsida. However, without disturbance effects colonization of sites created by Vallisneria by new species of Rotifera could have been unsuccessful. According to Shurin (2000) zooplankton communities are nearly saturated with species, thus biotic interactions may exclude many potential invaders. All the mentioned disturbances may thus weaken defense of native populations against invaders. They may also explain the successful expansion of more than 20 alien species in the system of Konin lakes. There are among them three species of bryozoans, crustaceans (Corophium robustrum (Sars), C. curvispinum (Sars), Echinogammarus ischnus (Strebbing), as many as seven species of mollusks (Sinanodonta woodiana (Lea), Potamopurgus antipodarum (Gray) and Physella acuta (Draparnaud), among others, and at least 6 species of fish (Kraszewski and Z danowski 2007). Results of the studies confirm the hypothesis that rare and new for Polish fauna rotifer species may appear in the littoral habitats of the heated Konin lakes and that the process is promoted by heating their waters and invasion of Vallisneria spiralis. However, the colonization of the habitats by rotifer invaders did not lead to their domination in the rotifer communities. ACKNOWLEDGEMENTS: The study was financially supported by the Polish Ministry of Science and Higher Education grant no. 2 PO4G 088 26. REFERENCES Baribwegure D., Segers H. 2001 Rotifera from Burundi: The Lepadellidae (Rotifera: Monogononta) Hydrobiologia, 446/447: 247 254 Czapik A. 1958 Wrotki (Rotatoria) okolic Krakowa [Rotifers (Rotatoria) in the vicinity of Cracow] Acta Zool. Cracoviensia, 3: 123 134. (in Polish). De Ridder M. 1985 Contributions to the knowledge of African Rotifers. I. Rotifers from Senegal Hydrobiologia, 120: 47 51 Ejsmont-Karabin J., Hutorowicz A. (in press) The effect of invasive Vallisneria spiralis L. (Hydrocharitaceae) on littoral communities of Rotifera in Konin lakes heated by power stations (W. Poland) Pol. J. Ecol. Elton C.S. 1958 The ecology of invasions by animals and plants Methuen & Co. Ltd., London. Heywood V.H. 1989 Patterns, extents, and modes of invasions by terrestrial plants (In: Biological Invasions: A Global Perspective, SCOPE 37. Eds: J.A. Drake, H.A. Mooney, F. di Castri, R.H. Groves, F.J. Kruger, M. Rejmanek, M.Williamson) Chichester, U.K. John Wiley & Sons Ltd Hillbricht-Ilkowska A., Ejsmont-Karabin J., Węgleńska T. 1988 Long-term changes in the composition, productivity and trophic efficiency in the zooplankton community of heated lakes near Konin (Poland) Ekol. pol. 36: 115 144. Hillbricht-Ilkowska A., Zdanowski B. 1988 Changes in lake ecosystems connected with the power-generating industry (the outline of problem); the Konin lakes (Poland) as the study sites Ekol. pol. 36: 5 21. Hutorowicz A. 2006 Vallisneria spiralis (Hydrocharitaceae) in lakes in the vicinity of Konin (Pojezierze Kujawskie) Biodiversity: Research and Conservation, 1 2: 154 158. Jose De Paggi S. 2002 Family Asplanchnidae Eckstein, 1883 (In: Rotifera 6: Asplanchnidae, Gastropodidae, Lindiidae, Microcodidae, Synchaetidae, Trichosphaeridae and Filinia. Eds: T.Nogrady, H. Segers) Guides to the Identification of the Micro-invertebrates of the Continental Waters of the World, 6, Backhuys Publishers, Leiden, pp. 1 27 Keast A. 1984 The introduced macrophyte, Myriophyllum spicatum, as a habitat for fish and their invertebrate prey Can. J. Zool. 62: 1289 1303. Kraszewski A., Zdanowski B. 2007 Sinanodonta woodiana (Lea, 1834) (Mollusca) a new mussel species in Poland: occurrence and habitat preferences in a heated lake system Pol. J. Ecol. 55: 337 356. Krull J.N. 1970 Aquatic plant-invertebrate associations and waterfowl J. Wildl. Manage. 34: 707 18.

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