ISSN 19950829, Inland Water Biology, 2011, Vol. 4, No. 1, pp. 39–46. © Pleiades Publishing, Ltd., 2011. Original Russian Text © S.M. Zhdanova, A.E. Dobrynin, 2011, published in Biologiya Vnutrennikh Vod, No. 1, 2011, pp. 45–52.

ZOOPLANKTON, ZOOBENTHOS, AND ZOOPERIPHYTON

Kellicotia bostoniensis (Rousselet, 1908) (Rotifera: ) in Waterbodies of European Russia S. M. Zhdanova and A. E. Dobrynin Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Nekouzskii raion, Yaroslavl oblast, 152742 Russia email: [email protected] Received April 14, 2009

Abstract—The bostoniensis (Rousselet, 1908), which is common in North American water bodies, has been recorded in 13 different lakes of the European part of Russia. A morphometric analysis has been made of populations from 7 lakes. The assumption has been made that the size of the spines of K. bos toniensis in small waterbodies depends on the presence of predators. Depthrelated changes in density and viscosity in deep lakes with temperature stratification can also influence this feature.

Keywords: Kellicottia bostoniensis, new locations, morphological variability, spatial distribution, waterbodies of European Russia. DOI: 10.1134/S1995082911010147

INTRODUCTION of the shell ranges from 400 to 1000 μm [28]. K. bos toniensis is known in the mineralized waterbodies of The genus Kellicottia Ahlstrom, 1938 (family Bra the Holarctic region [5]. The species has four unequal chionidae) includes two species, K. longispina (Kelli anterior spines (Fig. 1), and the length of the shell, cott, 1879) and K. bostoniensis (Rousselet, 1908) including the length of the spines, is ≤380 μm [28]. [5, 28]. K. longispina is a widespread inhabitant of It has been suggested [38] that K. bostoniensis is a waterbodies in northern latitudes. It is a pelagic limno nearctic species introduced into the paleoarctic philic euryhaline species [5]. The anterior dorsal edge region. This rotifer was first described in 1908 by of the lorica has six unpaired unequal spines. The cen Rousselet [35] in an artificial lake in Boston (United tral right spine is the longest and the left spine is much States). This species is common for the Great Lakes shorter. Lateral spines are rather long. The total length (Huron and Ontario) and bays, river mouths, and bogs

Fig. 1. Kellicottia bostoniensis from Lake Kshchara.

39 40 ZHDANOVA, DOBRYNIN of United States and Canada [15, 23]. It has also been surface. In lakes of the Valdai Hills (in Novgorod found in an oligotrophic acid lake in Canada [16]. It oblast), samples were collected with a Jedy net (with a occurs as a dominant species in some waterbodies of diameter at the mouth of 18 cm and a mesh size of Mexico [33]. Recent findings have been recorded in 64 μm from) from July 23–July 25, 2007. In Lake Brazil [29] and Argentina [17]. In Europe, K. bos Trestino (Tver oblast), the zooplankton was collected toniensis was first found in 1943 in a lake in Sweden in with a Jedy net (mouth opening of 12 cm and mesh the area of wastewater discharge from a pulp and paper size of 85 μm) from the bottom to the surface on mill [11]. Later, it was recorded in >11 lakes and rivers August 2, 2008. In Lake Kshchara (Vladimir oblast), of Sweden [11] and is considered a common species in the samples were collected with a Ruttner sampler 2 l the waterbodies of southern Sweden [26]. K. bos in volume at watercolumn depths of 0, 2, 4, 6, 7, 8, 10 toniensis was found in the Netherlands in 1960 in a and 12 m (three replicates from each layer) on Sep small mesotrophic pond with acid dark water [30]. tember 24, 2004. Then the samples were filtered This species has been documented in the Elbe and through a sieve with a mesh size of 64 μm. A total of Ems rivers in Germany [36, 37]. In Finland, it was first 29 samples were collected and processed. recorded in 1987 in Lake Tarjannevesi in areas weakly The morphological variability of K. bostoniensis was polluted by wastewaters [19, 23] and it entered the analyzed using 100 individuals from each sample. The dominating complex of zooplankton in small acid total length of the shell (ltotal), the length of the shell waterbodies [24, 27]. In France it was found in the (lshell) without spines, the length of the longest anterior humic acid lake Devesse [12]. In the territory of Rus (las), and the posterior (lps) spines were determined. The sia, it has been recorded only in two lakes in Leningrad measurements were conducted under a MBI3 light oblast [2]. In Asia, this rotifer has been found in some microscope equipped with an ocularmicrometer. The waterbodies of Japan [40]. stomach content of of the genus Asplanchna was The North America species K. bostoniensis has fixed in formalin and examined with a MBI3 light spread far from where it was first found. The distribu microscope. For an analysis of the morphological vari tion of K. bostoniensis is an example of biological inva ability of Kellicottia bostoniensis from Lake Kshchara, sion in fresh waters [18, 34]. This species was intro photographs of rotifers were taken under a Jenaval duced from North America to South America via the microscope (Karl Zeiss, Jena) with a Canon Power ballast waters of large ships and the transfer of the rest Shot A 72OIS digital camera. The scale was calibrated ing eggs of rotifers by migratory birds [31]. Its further by photographing a micrometer object at the same mag introduction into the waterbodies of Argentina and nification. The rotifers on the photographs were mea Brazil may occur through river systems [17]. The sured using Adobe Photoshop CS2. The data were pro appearance of K. bostoniensis in Europe, in particular, cessed using STATISTICA 6.0. A morphometrical in Sweden, is also caused by their transfer with ballast analysis was made of rotifers from the floodplain water waters and spreading in river basins and drainage bodies Lopata, Alekseevskoye, Nefedovo and Beloye channels [11]. and lakes Maloye Yaichko, Trestino, and Kshchara (at The total size of the K. bostoniensis shell varies in depths of 7, 8, 10, 12 m). The morphometrical param different waterbodies. In tropical regions individuals eters of K. bostoniensis from floodplain waterbodies of this species are smaller than in North American and Glushitsy, Aleshina Luka, and Sovkhozny vodopoi and European waterbodies [14]. lakes Bolshoye Yaichko, Glukhoye, Bragino, and Ksh The aim of this work is to describe new locations of chara (at depths of 0, 2, 4, 6 m) were not determined K. bostoniensis in the territory of European Russia and because of the low abundance of rotifers. study its morphological variability depending on envi ronmental conditions. RESULTS Kellicottia bostoniensis was documented by the MATERIALS AND METHODS authors in nine waterbodies of the central region (Rya The samples were collected in the course of hydro zan, Vladimir, and Tver oblasts) and in four lakes of the biological studies conducted in small lakes of the Val northwestern region of Russia (Novgorod oblast). dai Hills, in floodplain and in outoffloodplain New locations of the species: Ryazan oblast (flood waterbodies in the Oka Reserve (Ryazan Oblast), in plain waterbodies in the basins of the Pra and Oka riv karst lakes in Vladimir oblast, and in lakes of the Cen ers in the territory of the Oka Reserve: Lopata, Alek tral Forest Reserve (Tver Oblast). seevskoye, Glushitsy, Nefedovo, Beloye, Aleshina In the waterbodies of the Oka Reserve, zooplank Luka, and Sovkhozny vodopoi), Vladimir oblast (Lake ton samples were collected on July 7–12, 2007. At Kshchara), Tver oblast (Lake Trestino), and Novgorod depths of ≤1 m, 50 l of water collected with a bucket oblast (lakes Maloye Yaichko, Bolshoye Yaichko, from the surface layer was filtered through a plank Glukhoye, and Bragino). tonic net (mesh size of 85 μm). At depths of >1 m, a The waterbodies differ in origin and hydrochemical Jedy net (with a diameter at the mouth of 12 cm and a and hydrological characteristics. The floodplain mesh size of 85 μm) was set from the bottom to the waterbodies in the Oka Reserve are eutrophic, shallow

INLAND WATER BIOLOGY Vol. 4 No. 1 2011 Kellicotia bostoniensis (Rousselet, 1908) (Rotifera: Brachionidae) 41

Table 1. Characteristics of studied waterbodies

Coordinates of sampling site Waterbody Area, km2 Depth, m Transparency, m pH Color, grad NE Lopata 54°45′10.6′′ 40°59′54.5′′ 1.20 5 0.4 7.2 440 Alekseevskoye 54°44′14.3′′ 40°59′37.6′′ 0.03 1 0.4 6.7 440 Nefedovo 54°43′41.2′′ 40°58′01.6′′ 0.03 1 0.4 6.9 70 Beloye 54°42′48.2′′ 40°42′24.1′′ 0.01 1 0.3 6.9 380 Maloye Yaichko 57°36′52.9′′ 33°10′59.1′′ 0.30 4.2 0.75 5.6 170 Kshchara 56°24′52.9′′ 42°17′42.8′′ 1.14 12 2.4 7.6 35 Trestino 56°59′49′′ 32°30′46′′ 0.65 1 2 4.5 55

(1–4.2 m), neutral, mesohumic, and polyhumic (dark ferences (р = 0.05) in the size of individuals from the water) (Table 1). Karst lakes in the Valdai Hills studied waterbodies. The largest individuals were (Novgorod and Tver oblasts) are shallow, acid, poly found in lakes Maloye Yaichko and Trestino, and the and mesohumic, surrounded by bogs, and have no smallest ones were found in the floodplain waterbody runoff. Lake Kshchara is karst, deeper (a maximal Alekseevskoye (Table 3). depth of 12 m), stratified, mesotrophic [3], and oligo humic (light color of water) with neutral pH values of In Lake Kshchara, the size of rotifers varied water. During the survey, the thermocline was more depending on the depth (Table 3). The size of the shell expressed at horizons of 6–9 m and a slight fall of tem and spines of K. bostoniensis differed reliably (р = 0.05) perature was observed to a depth of 11 m (Fig. 2). The at horizons of 7–10 m (Table 3). The highest values of oxygen content varied from 8.6 mg/l near the surface morphometric parameters were found in individuals layer to 5.5 mg/l at a depth of 7 m and, at a depth of ≥10 m, a lack of oxygen was observed. 3 The abundance of K. bostoniensis in the studied g/m waterbodies varied several orders (Table 2). The maxi 1 2 3 mal density of the rotifer population was recorded in m Lake Kshchara (the upper part of the metalimnion), 0 and the minimal abundance was recorded in lakes of the Valdai Hills and the floodplain waterbodies Sovkhozny vodopoi and Glushitsy (Table 2). In differ ent waterbodies and in different areas and horizons, the species made up from 0.01 to 94% of the zooplank ton abundance. 4 In floodplain waterbodies in the basins of the rivers Pra and Oka, a high abundance of the species was 3 recorded in the littoral zone among macrophyte over 2 growths (Table 2). In waterbodies in the Valdai Hills, there was a high density of the K. bostoniensis popula 8 tion in central parts lacking higher aquatic vegetation (Table 2). 1 The vertical distribution of the species was studied using Lake Kshchara as an example. Low values of abundance were recorded in the epilimnion and on its boundary with the metalimnion (0–6 m) (Table 2). In 12 the upper part of the metalimnion (at a depth of 7 m), 7 11 15°C a sharp decrease in the rotifer concentrations was observed. In lower horizons (from 8 to 12 m), the 3 6 9 abundance of K. bostoniensis gradually decreased, but it was higher than in the epilimnion. mg/l Morphometric characteristic of the species. An Fig. 2. Vertical distribution of (1) temperature (°C), analysis of the morphometrical characteristics of (2) oxygen (mg/l), and (3) phytoplankton (g/m3) in Lake K. bostoniensis showed reliable interpopulational dif Kshchara; (ordinate axis) depth, m.

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Table 2. Abundance (thous. ind./m3) of Kellicottia bostonien gotrophic) and Lake Pionerskoye (mesotrophic). sis in the studied waterbodies These lakes are weakly acidic and stratified [9]. The rotifers were found there along the water column; the Waterbody Central part Littoral abundance of this species in Lake Pionerskoye 3 Lopata 1236.8 5.8 reached 10.8 million ind./m [2]. Findings of the species in different waterbodies Alekseevskoye 21.0 56.4 (shallow and deep, oligo and polyhumic, acidic and Glushitsy 0.1 – neutral, and mesotrophic and eutrophic) testify to the ability of the rotifer to spread widely in Eastern Nefedovo 0.8 603.0 Europe. Beloye 5.0 144.0 In the studied waterbodies, K. bostoniensis was found Aleshina Luka 0.7 8.0 along the water column; in deepwater Lake Kshchara, the rotifer preferred meta and hypolimnion water lay Sovkhozny vodopoi 0.1 0.0 ers, where the density of the population was 2–3 orders Maloye Yaichko 11.1 0.1 higher than in the epilimnion. This agrees with the data Bolshoye Yaichko 0.5 0.4 obtained by Ivanova and Telesh [2], who mentioned in their publication that, in October 2000, the abundance of Glukhoye 0.2 – K. bostoniensis in the epilimnion of Lake Pridorozhnoye 3 Bragino 1.6 0.1 amounted to 490 thous. ind./m and, in the hypolim nion, it reached 2 million ind./m3. Josefsson and Ander Kshchara: horizon 0 m 9.9 – sson [26] also showed that the rotifer was met numer 2 m 9.9 – ously in the nearbottom layers at low oxygen concen trations. This confirms their low demand for oxygen and 4 m 9.9 – ability to exist in low concentrations of it [25] in the 6 m 36.2 – hypolimnion of deep lakes [14, 19]. However, according 7 m 4363.3 – to Campbell’s data (cited in [19]), at the beginning of summer, K. bostoniensis is a hypolimnetic species, but 8 m 753.3 – the deficiency of oxygen in the hypolimnion makes 10 m 466.7 – individuals of the species migrate to the epilimnion. 12 m 166.7 – An analysis of the data has shown that individuals of K. bostoniensis from floodplain waterbodies in the Trestino 14.9 – Oka Reserve are smaller than individuals found in dif ferent waterbodies of Europe and North America (Table 3). The individuals of K. bostoniensis from lakes inhabiting the upper part of the metalimnion. Towards Maloye Yaichko and Trestino are similar in size to the hypolimnion, the sizes gradually decreased and individuals from the waterbodies of Europe and North increased again in the near bottom layer, reaching the America. size of individuals at the horizon of 8 m. Variations in the shell size of rotifers can be caused The contingency of morphometric features was by different factors: water temperature and its viscos estimated by the coefficients of correlation (Table 4). ity, the amount of food [10], the abundance of rotifers, The correlation between the length of spines and the and the presence of predators [13]. length of the shell was almost negligible and, in some The effect of biotic factors on the morphological cases, the coefficient of correlation had negative val variability of some rotifers, namely, the presence of ues. A stronger positive correlation was found between predators, was first mentioned by Beauchamp [13]. the length of the anterior and posterior spines. The During the experiment he observed that, in the pres coefficient of correlation was reliable (p = 0.05) in all ence of Asplanchna priodonta Gosse, the posterior lat waterbodies and horizons and varied from 0.34 to 0.72. eral spines of the shell of calyciflorus Pallas On the whole, a strong correlation (r = 0.81, p < 0.001) became longer. An analysis of the relations between was found in individuals from the floodplain water rotifers (predators Asplanchna girodi Guerne and bodies of the Oka Reserve and a significant correlation A. sieboldi (Leydig) and prey (r = 0.68, p = 0.001) was found in rotifers from Lake and B. rubens Ehrenberg) in the experiment and in nat Kshchara. ural waterbodies confirmed this dependence [20, 21, 41]. Variations in the spine length of B. calyciflorus were related to the Asplanchna population density and DISCUSSION depended on the concentration of a special inducing Findings of K. bostoniensis on the territory of Rus substance of the protein origin extracted by it. sia were recorded in two small freshwater lakes in Len The small size of Kellicottia bostoniensis in tropical ingrad oblast in 2000 [2]: in Lake Pridorozhnoye (oli waterbodies is explained by its recent introduction and

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Table 3. Morphometrical indices of Kellicottia bostoniensis

ltotal lshell las lps Water object n Literature source μm Floodplain waterbodies: 335± 2.0 107± 0.0 133± 1.0 94± 1.0 Lopata 100 Authors’ data 269–381 94–128 94–158 72–114 273± 2.0 106± 0.0 93± 1.0 73± 1.0 Alekseevskoye 100 The same 234–333 94–117 72–122 56–100 309± 2.0 105± 0.0 119± 1.0 86± 1.0 Nefedovo 100 '' 256–358 97–117 91–147 61–111 Lakes: 312± 2.0 104± 0.0 122± 1.0 86± 1.0 Beloye 100 '' 258–369 92–111 97–147 56–117 380± 2.0 110± 0.0 145± 1.0 123± 1.0 Maloye Yaichko 100 '' 331–456 100–119 122–175 103–167 368± 2.1 102± 0.8 150± 1.3 117± 1.2 Kshchara: horizon of 7 m 100 '' 297–427 80–128 79–172 79–168 325± 1.6 89± 0.7 133± 0.9 103± 1.0 8 m 100 '' 278–367 68–109 93–155 75–128 296± 2.1 83± 0.7 119± 0.9 94± 1.0 10 m 100 '' 249–352 60–111 96–142 72–122 320± 1.9 91± 0.6 127± 1.0 102± 1.0 12 m 100 '' 267–359 71–112 97–154 79–128 379± 0.0 112± 0.0 143± 0.0 124± 0.0 Trestino 100 '' 319–439 100–119 111–166 89–152 380 – 150 130 Vattern (Sweden) 100 [11] – – – – 360 – 136 128 Lake (United States) – [11] – – – – 368± 3.3 107± 2.0 – – Star (United States) – [22] – – – – 381± 5.0 – – 125± 6.0 Tarjannevesi (Finland) 20 [19] 340–415 – 130–170 100–170 374± 2.0 109± 1.0 139± 1.0 123± 1.0 Devesse (France) 51 [12] – – – – 285± 2.0 105± 1.0 108± 1 74± 1.0 Nadu (Brazil)65 [14] – – – – 306± 3.0 101± 1.0 115± 1 90± 2.0 Furnas Reservoir (Brazil) 55 [14] – – – – – – – – Basin of the Tiete River (Brazil) – [32] 270–410 – 110–160 60–120 Note: The mean value and its error is shown above the line, the range of variations is under the line, and n is the number of individuals in collected samples.

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Table 4. Coefficients of correlation between the length of the spines of Kellicottia bostoniensis is larger (Table 3) than shell and the length of anterior and posterior spines of Kellicot in floodplain waterbodies Alekseevskoye and Nefe tia bostoniensis dovo, where those species were not recorded. Coefficients of correlation In Lake Kshchara, a coincidence between the verti Waterbody cal distribution of K. bostoniensis and copepodites of lshelllas lshelllps laslps cyclopids (r = 0.92, p = 0.001) was recorded. As in the Lopata 0.18 0.25 0.57 case of rotifers, the maximum of the abundance of juve nile copepodids was recorded at a depth of 7 m. The lat Alekseevskoye 0.38 0.17 0.52 ter were mainly represented by copepodites III–IV of Nefedovo –0.04 0.22 0.65 the predator–grabber Mesocyclops leuckari Claus, Beloye 0.09 0.12 0.61 which are similar to adult individuals in regards to mode Maloye Yaichko 0.29 0.41 0.69 of feeding [1, 6]. Unfortunately, analyzing the intestines of cyclopid copepodites is difficult because they do not Trestino 0.12 0.26 0.72 consume their prey in whole or in part, but only their Kshchara: horizon of 7 m 0.09 –0.18 0.34 contents [7]. Thus, in spite of the low mobility of Kelli 8 m –0.21 –0.14 0.34 cottia bostoniensis, the larger size of its shell and spines can protect it from being eaten. 10 m 0.28 0.30 0.70 12 m –0.01 –0.04 0.54 In Lake Kshchara at depths of 7–10 m, the decrease in temperature from 12.6 to 8.4°С led to a For all populations 0.15 0.15 0.80 decrease in the water density and viscosity. Therefore, Note: Reliable values (p = 0.05) are in bold. spines played a smaller role as a tool for hovering at lower horizons. The increase in size of K. bostoniensis in the nearbottom layer (at 12 m) is probably related the absence of a selective predator rotifer of the genus to the presence of predatory larvae Chaoborus crystal Asplanchna [14]. Rotifers of this genus are able to con linus (De Geer) (according to our data and [8]), which sume Kellicottia bostoniensis [39]. In the studied water were not found in the above layers. bodies, the genus Asplanchna is represented by A. pri odonta (a body size of 0.40–0.92 mm), A. Henrietta In Lake Kshchara, the presence of size groups of Langhans (0.41–0.51 mm), A. herricki Guerne Kellicottia bostoniensis differed significantly can testify (0.69 mm), and A. brightwelli Gosse (1.11 mm). An to the formation of its subpopulations at different analysis of the intestine content of Kellicottia bos horizons and the low daily migratory activity of indi toniensis showed that Asplanchna priodonta and viduals of the species. A. henrietta did not consume Kellicottia (Table 5). In Based on data on the contingency of morphomet Lake Kshchara, predators and prey were separated ric features, we can suggest that, under unfavorable spatially. Mediumsized (0.4 ± 0.1 mm) Asplanchna conditions, the tendency to increase in body size at priodonta inhabited the epilimnion with the maximal 3 populational and subpopulational levels depends to a abundance (7.8 thous. ind./m ) at the horizon of 4 m greater degree on the individual variability of rotifers. and was absent at depths >6 m, where Kellicottia was The regression coefficients of the ratio between the mainly concentrated. length of the anterior and posterior spines obtained by K. bostoniensis was often found in the stomachs of Schulz [37] for K. bostoniensis from the Ems River Asplanchna herricki and A. brightwelli (Table 5). The (Germany) are similar. For individuals from the Ems portion of in the food of A. herricki and River, lengthening of the anterior spine by 1 μm A. brightwelli was higher than of A. priodonta and increases the posterior spine by 0.7 μm; for individuals A.henrietta [4]. In the floodplain waterbody Lopata from floodplain waterbodies of the Oka Reserve, such and in Lake Maloye Yaichko, which are inhabited by an increase constituted 0.85 μm; and from Lake A. herricki and A. brightwelli, the size of the shell and Kshara, it was 0.72 μm.

Table 5. Occurrence (%) of Kellicottia bostoniensis in the stomachs of representatives of the genus Asplanchna Waterbodies Species Alekseevskoye Nefedovo Lopata Maloye Yaichko Kshchara Trestino A. priodonta 00–200 A. henrietta 0– 1––– A. brightwelli ––48––– A. herricki –––46––

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CONCLUSIONS tent Patterns of Hydrobiological Regime of Water Bodies of Different Types), Moscow: Nauch. Mir, 2004, New localities of North American species K. bos pp. 11–15. toniensis, which are rare for Russia, have been found. 10. Erman, L.A., Cyclomorphosis and Feeding of Plank These rotifers were recorded in different (shallow and tonic Rotifers, Zool. Zh., 1962, vol. 41, no. 7, pp. 998– deep; floodplain and unflooded; mesotrophic and 1003. eutrophic; oligoacid and neutral; and oligo, meso 11. Arnemo, R., Berzins, B., Gronberg, B., and Mellgren, I., and polyhumic) waterbodies in Ryazan, Vladimir, Tver The Dispersal in Swedish Waters of Kellicottia bos and, Novgorod oblasts. Their abundance varied from (Rousselet) (Rotatoria), , 1968, vol. 19, 3 3 toniensis Oikos 100 ind./m up to 4.36 million ind./m . The total body no. 2, pp. 351–358. μ size of K. bostoniensis ranged from 234 to 456 m. 12. Balvay, G., First Record of the Rotifer Kellicottia bos It has been found that the ratio between the length toniensis (Rousselet, 1908) in France, J. Plankton Res., of the anterior and posterior spines is larger than the 1994, vol. 16, no. 8, pp. 1071–1074. ratio between the length of the spines and the length of 13. Beauchamp, P., Classe des Rotifers, Traite de Zoologie, the shell. In shallow waterbodies, the length of spines Anatomie, Systematique, Biologie, 1965, vol. 4, no. 3, of K. bostoniensis depends mainly on the presence of pp. 1225–1379. predators. In deepwater lakes with temperature strat 14. BezerraNeto, J.F., Aguila, L.R., Landa, G.G., and ification, the changes in density and viscosity of water PintoCoelho, R.M., The Exotic Rotifer Kellicottia at deeper layers can also influence the length of spines. bostoniensis (Rousselet, 1908) (Rotifera: Brachionidae) in the Zooplankton Community in a Tropical Reser voir, Lundiana, 2004, vol. 5, no. 2, pp. 151–153. REFERENCES 15. 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