CC BY
18Journal of Siberian Federal University. Biology 1 (2015 8) 66-84
УДК 574.583
Plankton Community in the Pelagic and Littoral Zones of the Overgrown Lake Beloe
(Volzhsko-Kamskiy Biosphere Natural State Reserve, Republic of Tatarstan, Russian Federation)
Oksana V. Mukhortovaa*, Svetlana V. Bykovaa, Natalia G. Tarasovaa, Elena N. Unkovskayab and Sergey E. Bolotovc
a Institute of Ecology of the Volga River Basin RAS 10 Komzina, Togliatti, 445003, Russia b Volzhsko-Kamskiy Biosphere Natural State Reserve Sadovyi, Raifa, Zelenodolskiy District, Republic of Tatarstan, 422537, Russia c Institute for Biology of Inland Waters RAS Borok, 152742, Russia
Received 16.10.2014, received in revised form 20.12.2014, accepted 09.02.2015 Comparative analysis of different groups of the planktonic community (phytoplankton, protozoo- and zooplankton) was performed in the pelagic and littoral zones of overgrown Lake Beloe (Volzhsko-Kamskiy Biosphere Natural State Reserve, Republic of Tatarstan, Russain Federation). We detected a remarkable diversity of both pelagic and sublittoral plankton. The planktonic community of the macrophyte zone differs from the community of pelagic zone in a species composition and in larger species diversity.
Keywords: protozooplankton, zooplankton, phytoplankton, planktonic community, abundance, biomass, macrophytes.
© Siberian Federal University. All rights reserved
* Corresponding author E-mail address: muhortova-o@mail.ru
Характеристика планктонного сообщества пелагической и литоральной зоны зарастающего мезотрофного озера Белое (Волжско-Камский биосферный природный государственный заповедник, Республика Татарстан)
О.В. Мухортоваа*, С.В. Быкова3, Н.Г. Тарасова8, Е.Н. Унковская6, С.Э. Болотов"
аИнститут экологии Волжского бассейна РАН Россия, 445003, Тольятти, ул. Комзина, 10 бВолжско-Камский государственный природный биосферный заповедник, Россия, 422537, Республика Татарстан, Зеленодольский район, п. Садовый вИнститут биологии внутренних вод им. И.Д. Папанина РАН
Россия, 152742, п. Борок
Проведен сравнительный анализ развития планктонных организмов (фито-, зоо-, протозоопланктон) в пелагической и литоральной зоне зарастающего озера Белого (Волжско-Камский биосферный природный государственный заповедник, Республика Татарстан). Показано, что в макрофитах все компоненты планктонного сообщества отличаются большим, по сравнению с пелагиалью, видовым богатством и значительной видоспецифичностью. Отмечено значительное различие состава пелагического и зарослевого планктона. Планктонные сообщества водной толщи, обитающие в зарослях различных видов макрофитов, отличались меньше.
Ключевые слова: протозоопланктон, фитопланктон, зоопланктон, планктонное сообщество, численность, биомасса, макрофиты.
Introduction
The littoral zone of a lake is known to be an area with a specific complex of conditions that influences the entire lake ecosystem (Nurminen, 2003; Carpenter et al., 1992; Schindler et al.,
1996). Macrophytes are an important component in regulating the biological structure of a lake (Timms, Moss, 1984; Schriver et al., 1995). Macrophytes influence organism distribution in a lake (Durte et al., 1986; Moddelboe, Markager,
1997), light transmission, temperature and pH (Dale, 1986; Duarte et al., 1986; Vant et al., 1986, 1995, 1996; Lodge, 1991).
Macrophyte occurrence in a lake and degree of its overgrowth show trophic conditions of a lake (Schulthorpe, 1967; Toivonen, Huttunen, 1995). Complex relations between planktonic organisms and between planktonic organisms and macrophytes are a subject matter and a basis for making hypothesis and theories for different scientists (Scheffer et al., 1993, 1992; Jeppesen et al., 1998).
Usually, sublittoral planktonic community in the macrophy te zone differs from that in the pelagic zone of a water body and consists of truly planktonic as well as of
the periphytic and benthonic species (Barko, James 1999; Karabin, 1985; Lauridsen et al., 1996; Persson, 1991). Macrophytes form a community habitat and establish development peculiarities of all groups of planktonic community (particularly, protozoo-, zoo-and phytoplankton) in a littoral zone of a lake with macrovegetation (Nurminen et al., 2001). The problem of planktonic organisms development in macrovegetation is not limited to clearing up differences in biodiversity indicators in various biotopes for diverse planktonic components, but it also involves a study of interaction between macrovegetation and planktonic community as a whole. The interaction is reflected by a competition, by displacing a competitor in space, light interception (shading) or nutrient interception (intensive absorption), by allelopathic influence (Fairchild, 1981; Lauridsen et al., 1997; Nabivaiylo, Titlyanov, 2006; Nurminen, 2003), by interspecific competition of zooplankton in macrovegetation, by influence of invertebrate predators inter-connected with macrovegetation on zooplankton (Horppila, Nurminen, 2001, 2003; Semenchenko, 2006). Besides, this interaction affects structural and productional indicators of the whole planktonic community.
The first stage in research of any problem (particularly, revealing of interaction mechanism) consists of data accumulation. In this instance, phyto -, protozoo - and zooplankton are researched in various ecotopes diverse in mineralization, chemical structure, the extent of overgrowth and morphometry of various lakes. This work presents the results of the first planktonic community research in macrovegetation of Lake Beloe. The study is intended to identify peculiarities of planktonic community development (as a whole and its separate components), comparing a pelagic part
of basin with a littoral one and associations formed by particular macrovegetation species.
Materials and methods
Study site
Lake Beloe (55°55'26.2''N, 48°45'49.9''E) is located in a protected zone of the Raifskiy area of Volzhsko-Kamskiy State Natural Biospheric reserve, Republic of Tatarstan, Russian Federation. It is located in a hydrosystem of the rivers Sumka and Ser-Bulak, located in a karst-suffosion valley (Fig. 1).
Lake Beloe is a water body of karst-suffosion origin, overgrown (30 % of its area is occupied by macrophytes located along the coastal zone). Water retention time in the lake is high, its maximum depth of 4 m, which is found in the south-eastern part of the lake (Fig. 2). The lake length is about 557 m and its width is about 170 m. At the sampling time, the lake was thermally stratified with a thermocline at the depth of 2-3 m. Water transparency was up to 1.4 m and water colour value was low (80°Pt).
Lake water has medium level of mineralization and belongs to calcium-hydrocarbonate type. In 2006, a surface layer was oxygen saturated (up to 168 %), while we revealed a saturation deficit (8.7 %) at the bottom. The following macrophytes are located in the 10 m width littoral zone: Typha latifolia L., Zizania latifolia Stapf. and Sagittaria sagittifolia L. A shallow part of the lake, with a depth of less than 1 m, is covered by Ceratophyllum demersum L., Elodea canadensis Michx., Potamogeton angustifolius J.Presl and Nuphar lutea L.
Sampling
Our study of the planktonic community (phyto-, zooplankton, ciliates) was conducted in July of 2006 in six different biotopes: a) a water column in the pelagic part, and b) in a macrovegetation, belonging to different
Lake Kasanskoe
Fig. 1. System of lakes located in the protective zone of Raifskiy area of the Volzhsko-Kamskiy State Natural Biospheric reserve, Republic of Tatarstan, Russia
Fig . 2. Bathymetric map and photo of Lake Beloe
ecological types (Papchenkov, 2006): helophyte tall grass (Z. latifolia) and helophyte low-grass (S. sagittifolia), submerged rooted hydrophytes (C. demersum and P. angustifolius) and rooted hydrophytes with floating leaves (N. lutea).
Samples were collected with Ruttner bathometer (4 L). In macrophyte beds water was sampled from a surface layer (0.1-0.3 m). In the pelagic zone samples for phyto- and protozooplankton analyses and zooplankton analyses were taken from a surface layer (0.1-0.3 m) and from the whole water column (0-4 m), respectively.
Phytoplankton analysis
Phytoplankton was c oncenirated by filtering 0.5 L of sample through membrane filters of 1 |m pore diameter using Komovskiy pump and fixed in 4 % formalin. Cells calculation was made in Uchinskaya chamber (0.01 ml volume). Algae biomass was determined with geometric figures method (Kouzmin, 1984). Algae identification was made using standard guidebooks from the series "Susswasserflora von Mitteleuropa" (Ettl, 1983; Ettl, Gartner, 1983; Etel et ail., 1990; Hdlawell, 1986; Husted, 1939; Krammee, Lange-Beetalot, 1986, 1988, 1991a, 19911); Komarek, Anagnostidi, 2000; Popovsky, Pfiester, 1990; Starmach, 1985; Systematik und Biologie, 1983).
Protozooplankton analysis
Only ciliates from the group of prolozoa were studied in this research. Ciliates were identified i n alive state, or using samples fixed with mercury chloride (HgCl2) and in vapors of osmium. We also used impregnation by silver nitrate (AgNO3) (Chatton, Lwoff, 1936) and Feulgen nuclear staining. For species identification we used guide books as well as different papers (Corliss, 1979; Curds et al., 1982, 1983; Foissner et al., 1991, 1999; Kahl, 1931-1935). Counting of planktonic ciliates was performed after concentoation 300
ml of a sample (Mamaeva, 1979) and its fixation with saturated solution of mercury chloride (HgCl2). The results were generalized according to taxonomic system of E.B. Small and D.H. Lynn (1985, 2000), taking into consideration other literature sources (Yankovski, 2007). The trophic groups of ciliates were determined based on Pratt and Cairns (1985), Mamayeva (1979) and Zharikov (1996).
Zooplankton analysis
For zooplankton analysis we concentrated 5 L of water by filtering it through Apstein net of 64 |m mesi size. ZoopOankton samplet were fixed with 4 % Oormalin and counted in tiit Bogorov chamber. Abundance (ind.iL) and biomass (mg/m3) were calculated for each species in each sample. The tables of standart weights of organisms (Morduhay-Boltovskoy, 1954) and our measurements were used to calculate the biomass. The average length of ihe body was converted tn weight by method of Vinberg (1971)) and Balushkina & Vinberg (1979). The guide books of Kutikova (1970, 2005), Manuylova (1964), Smirnov (1976, 1996) and Orlo°a-Bienkowskaja (21001) were used iaa identification of the zooplankters.
Data analysis
If every group (phytoplankton, protozooplankton, zooplankton) we considered as dominant species those with abundance and biomass nof less than 10 % of o total abunfanci and biomass (Belova, 1998).
Species diversity was evaluated using Shannon index (Odum, 1975):
"-*[( 2) - (N)]
where: Ni - the abundance of species (i); N - the total abundance ofall species (W).
Pielou index was used for confirmation of species community equitability on abundance:
E = H/log N
where N - species community abundance in biocenosis (Odum, 1975).
Simklarity oV the planktonic communities in different ecotopes was calvu lated with S0rensen's similarity coefficient:
a + b
where a - the number of species in the first ecotope, b - the number of species in the second ecotope, c - the number of species common to both ecotopes (Odum, 1975).
Stand Density Index (SDI) was calculated for each species in community. SDI is the criteria, connecting average biomass (OB) and the abundance erf individuals (TV), characterizing species inside of biocoenosis (Dedyu, 1989):
sdi = 4nb
To study the variations of plankton community, a principal component analysis (PCA) was conducted. A PCA was made for the total community on the basis of Stand Density gndex.
Cluster analysis was made using S0rensen's similarity coefficient for planktonic communities in different ecotopes. Clustering of data was made by Ward method, eucledean distance was used as grouping parameter.
Statistical analysis (data clusterization and factor analysis) of the results was made using Statistica software, version 6.0 (StatSoft Inc., USA).
Plotting oO a bathy merric map of the Lake Beloe was executed in the program Surfer 12 (Golden Software Inc., USA).
Results and discussion
Species diversity and species specificity of planktonic community in different biotopes
In 2006 in all biotopes we found 116 species of phytoplankton, 57 species of protozooplankton and 84 species of zooplankton (taking into account phyto- and protozooplankton inhabiting a surface layer of the pelagic zone and zooplankton inhabiting the whole water column of the pelagic zone). Among them, 17 % of phytoplankton species, 14 % of ciliate species and 18 % of zooplankton species were unique for pelagic zone and 47 % of phytoplankton species, 68 % of ciliate species and 60 % of zooplankton species were unique for the macrophyte zone. Similarities between pelagic and macrophyte zones were 55 % for phytoplankton community, 30 % for ciliates and 35 % for zooplankton community. S0rensen's coefficients indicated low similarity between plankton inhabiting pelagic zone and communities of different sublittoral ecotopes (3445 % - for phytoplankton, 12-19 % - for ciliate, 45-57 % - for zooplankton). From the other side, similarity between plankton communities inhabiting different macrophyte species beds was high (4П-66 % - for phytoplankton, 55-68 % -for ciliate, 44-50 % - for zooplankton). Cluster analysi- indicated the peculiarity of pelagic plankton; and the community from Nuphar was the closest to the pelagic one among the sublitoral ecotopes (Fig. 3). Species diversity of zooplankton (Shannon index based on abundance Hn = 4.59; Pielou index E = 0.84) and phytoplankton (Hn = 4.76; E = 0.78) community was higher in the zone of submerged rooted macrophytes (Ceratophyllum and Potamogeton). Shannon index was high due to a high number of species and a relatively lownumber of dominant species (or even their absence) (Table 1).
Only two dominants were registered in the phytoplankton community of P. angustifolius -
Wirf s rWIfOÎ EucldcsTi (isür^.ri
Fig. 3. Cluster analysis on similarity of the communities (phyto-, protozoo- and zooplankton) in Lake Beloe Table 1: Comparison of plankton in different zones of Lake Beloe in July 2006
Biotope
Parameter Groups of plankton Pelagial, surface layer (0.3 m) Nuphar lutea Potamogeton angustifolius Ceratophyllum demersum Sagittaria sagittifolia Zizania latifolia
Phytoplankton 27 35 69 49 30 33
Number of species Protozooplankton c 9 24 23 25 34 n.f.
Zooplankton n.d. 22 n.f. 44 24 37
Shannon index, Ha a /Hbb Phytoplankton Protozooplankton 3.9/2.2 1.8/1.6 3.79/2.74 2.55/3.34 4.76/3.38 2.11/3.24 4.28/2.56 1.99/1.94 1.63/3.17 2.83/3.42 2.64/2.40 n.f.
Zooplankton n.d. 3.0/2.56 n.f. 4.59/3.86 4.17/3.26 4.18/3.01
Phytoplankton 0.82 0.74 0.78 0.76 0.33 0.52
Pielou index, E Protozooplankton 0.57 0.56 0.47 0.43 0.56 n.f.
Zooplankton n.d. 0.67 n.f. 0.84 0.91 0.80
Phytoplankton 1896000 1952000 6316000 3560000 4840000 4588000
Abundance, ind./L Protozooplankton 1006.5 1079.1 5349.3 30610.8 9810.9 n.f.
Zooplankton n.d. 266.8 n.f. 469.2 702 651.8
Phytoplankton 1642.2 1868.6 8006.6 7873.1 1037.5 5910.3
Biomass, mg/m3 Protozooplankton 35 19.9 55.9 457.8 116.2 n.f.
Zooplankton n.d. 1583.8 n.f. 3218.2 20745.4 11324.9
n.d. - not determined n.f. - not found
■ Shannon index calculated based on abundance b Shannon index calculated based on biomass c Protozooplankton = Ciliates
Pseudoanabaena limnetica (Lemmermann) Komarek (14 % of total abundance) and Eudorina elegans Ehrenberg (12 %). In zooplankton community from C. demersum, 94 % of total abundance was presented by subdominants, while dominants were absent. The maximum Shannon index for ciliates (Hn = 2.83; E = 0.56) was registered in S. sagittifolia zone (Table 1).
Characteristics of general quantity parameters of planktonic community
Maximum total abundance (4.85 x 106 ind./L) and biomass (21.89 mg/L) for phyto-, protozoo-and zooplankton (from macrophyte association of three different ecotypes: N. lutea, C. demersum and S. sagittifolia) were registered for the zone of S. sagittifolia. Maximum total number of species (118 species) was registered for planktonic community in C. demersum. Maximum numbers of plankton species were registered in different biotopes: for phytoplankton and zooplankton - in submerged rooted hydrophytes zone; for ciliates -in low-grasses helophyte zone (Table 1). High abundance and biomass of plankton in submerged rooted plants communities was noticed previously (Bykova et al., 2009; Mukhortova, 2008; Tarasova, 2008; Unkovskaya et al., 2010). It is explained by (1) presence of a suspended organic matter and fine detritus, (2) better protection from waves and wind, (3) diversity of local niches etc. Maximum value of zooplankton abundance in S. sagittifolia was caused by a great number of nauplii there. Minimum number of species (81), total abundance (1.95 x 106 ind./L) and total biomass (3.47 mg/L) were registered in N. lutea zone. It's interesting that species inhabiting this zone were similar to those in pelagic zone, because the N. lutea forms the most "pelagic" zone of macrophytes. As it is also known, this plant extracts the alkaloid nupharin, depressing the development of cyanophyta (Lauridsen et al., 1997; Zimbalevskaya, 1981). Furthermore, broad
leaves of N. lutea reduce the light penetration to the water column and due to this unfavorable for the phytoplankton. Lack of available food decreases number of protozoan (ciliates) and metazoan plankton species.
Structure of plankton in different zones
Chlorophyta was the only group dominating in phytoplankton of all zones in 2006 (Table 2). The abundance of Chlorophyta was maximum in the pelagic zone and in the Z. latifolia zone that was correlated with the complete absence of cyanobacteria there. However the dominants inside the group were different in different zones: Eutetramorus planctonicus (Korsch.) Bourrelly (19.4 % of total abundance) and Eudorina elegans Her. (18.1 %) in pelagic zone; E. planctonicus was absent in Z. latifolia, while abundance of E. elegans was 54 % of total.
Phytoplankton in 2006 was characterized by a lack of cyanoprokaryota in pelagic zone and its maximum ability (76 % of total abundance) in S. sagittifolia community due to a single species, Microcystis pulverea (Wood) Forti emend. Elenk. In Kuibyshev reservoir, a large water body located near Lake Beloe, M. pulverea causes water blooms. We assume that in Lake Beloe bloom of M. pulverea probably started to develop just in a warm, shallow zone of Sagittaria community. However due to the fact that small-celled Microcystis (cell diameter -1 ^m; colony diameter - less than 20 ^m) was probably consumed by nauplii (Jeppesen et al., 1992; Kerfoot et al., 1988; Kryuchkova, 1989), this bloom did not spread. In other macrophyte communities, blue-green algae were presented by attached forms Oscillatoria, Lyngbia, Phormidium etc., which could be a food for secondary filterers, cladocerans. The number of attached algae was especially high in the plankton inhabiting macrophytes having broad leaves (S. sagittifolia, N. lutea).
Table 2: The dominant species of phytoplankton, protozoo- and zooplankton in different biotopes of Lake Beloe in July 2006
Biotope Dominant on abundance Dominant on biomass
1 2 3
Phytoplankton
Surface layer (0.3 m)
Nuphar lutea
Potamogeton angustifolius
Ceratophyllum demersum
Sagittaria sagittifolia
Zizania latifolia
Protozooplankton Surface layer (0.3 m)
Nuphar lutea
Potamogeton angustifolius
Ceratophyllum demersum Sagittaria sagittifolia
Eutetramorusplanctonicus (19) *; Eudorina elegans (18); Syncripta volvox Ehr. (17); Stephanodiscus hantzschii Grun. (11); Dinobrion divergens Imgh. (11) Planctolyngbya limnetica (Lemm.) Kom.-Leg. et Cron. (18); Eudorina elegans (16); Dinobrion divergens (14); Stephanodiscus hantzschii (12)
Pseudoanabaena limnetica (Lemm.) Kom. (14); Eudorina elegans (12)
Cyclotella meneghengiana Kutz. (20); Leptolyngbya fragilis (Gom.) Angnostidis et Komárek (19) Microcystis pulverea (76)
Eudorina elegans (54)
Litonotus sp. (50)*; Peritricha spp. in Bosmina (39) Halteria grandinella (O.F. Muller, 1773) (47); Ctedoctema acanthocrypta Stokes, 1884 (27)
Ctedoctema acanthocrypta (63); Halterio grandinella (12)
Coleps hirtus (Muller, 1786) Nitzsch, 1827 (57)
Ctedoctema acanthocrypta (37); Coleps hirtus (17); Halterio grandinella (14)
Stephanodiscus hantzschii (54); Dinobrion divergens (11); Eudorina elegans (10)
Stephanodiscus hantzschii (56); Eudorina elegans (14); Dinobrion divergens (13)
Cosmarium cyclum Lund. var. articum Nordst. (35); Stephanodiscus hantzschii (22)
Cosmarium cyclum var. articum (50); Cyclotella meneghengiana (22)
Dinobrion divergens (33); Eudorina elegans (19); Stephanodiscus hantzschii (14); Gyrosigma kuetzingii (Grun.) CI. (10) Eudorina elegans (37); Stephanodiscus hantzschii (33); Melosira varians Agardh 1827 (11)
Paradileptus conicus Wenrich, 1929 (81); Litonotus sp. (11) Halterio grandinella (25); Ophryoglena sp. (16); Amphileptus pleurosigma (Stokes, 1884) (19)
Ctedoctema acanthocrypta (24); Lembadion lucens Maskell, 1877 (15); Strobilidium caudatum (Fromentel, 1876) (12); Halterio grandinella (11)
Coleps hirtus (57); Furgasonia trichocystis (Stokes, 1894) (13)
Coleps hirtus (22); Lembadion lucens (22); Ctedoctema acanthocrypta (13); Halterio grandinella (12)
Continuation Table. 2
1 2 3
Zooplankton
Surface layer (0.3 m) ad. ad.
Nuphar lutea Chydorus sphaericus (O.F. Muller, 1776) (13); Ceriodaphnia reticulata (Jurine, 1820) (12); nauplius Cyclopoida (22) Cyclopoida copepodites III-IV (41); Cyclopoida copepodites I-II (21); Simocephalus vetulus (O.F. Muller,1776) (10); Ceriodaphnia reticulata (12)
Potamogeton angustifolius n.f. n.f.
Ceratophyllum demersum - Cyclopoida copepodites III-IV (21); Mesocyclops leuckarti (Claus, 1857) (13);
Sagittaria sagittifolia nauplius Cyclopoida (11) Cyclopoida copepodites III-IV (33)
Zizania latifolia nauplius Cyclopoida (11); Ceriodaphnia reticulata (12) Mesocyclops leuckarti (35); Acanthocyclops vernalis (Fischer, 1853) (10); Eucyclops macruroides (Lilljeborg, 1901) (20)
* In parentheses we indicated the abundance of species (in percent of the total abundance or biomass); «-» - absence of dominant species (> 10 % of total abundance or biomass); n.d. - not determined n.f. - not found
Another peculiarity of the plankton of Lake Beloe in 2006 was a relatively high number of Rotifera in pelagic zooplankton (44 %) comparing with littoral community (11-24 %). Our results are in a good agreement with those by O.Yu. Derevenskaya (2002), who also found high abundance of Rotifera in the pelagic zone of Lake Beloe. As Rotiferia prefer more eutrophic conditions, we can propose that in the littoral zone macrophytes adsorb the organic particles from the water, but there is a lot of fine detritus on the leaves surface. It could be regarded as explanation of high number of the sessile rotifers Rotaria neptunia (Ehrenberg, 1832), R. rotatoria rotatoria (Pallas, 1766), Dissotrocha aculeata aculeata (Ehrenberg, 1832) and scrapping crustaceans (Pleuroxus truncatus (O.F. Müller, 1785), P. aduncus (Jurine, 1820), Chydorus sphaericus (O.F. Müller, 1785), C. ovalis Kurz, 1875, Alona intermedia Sars, 1862, Alona rectangula Sars, 1861) occasionally present in plankton samples. These species generally are filterers. They were washed out from the floating leaves of Nuphar lutea and gave about 94 % of "plankton" abundance. In zooplankton inhabiting other macrophytes (Typha latifolia, Zizania latifolia, Sagittaria sagittifolia, Ceratophyllum demersum, Elodea Canadensis and Potamogeton angustifolius) and in the pelagic zooplankton the percentage of filterers was lower (68-80 % of total abundance) and the role of predators (Mesocyclops leuckarti (Claus, 1857), Thermocyclops oithonoides (Sars G.O., 1862), Eucyclops macruroides (Lilljeborg, 1901), Microcyclops varicans (Sars G.O., 1863)) was more considerable. Some authors (Lauridsen et al., 1997; Zimbalevskaya, 1981) observed similar distribution of filterers and predators in zooplankton community.
Ciliate community was characterized by the dominance of predators in pelagic plankton (54 % of total number and 92 % of total biomass). In macrophyte zone, besides bacteriodetritophages,
the dominants in the plankton were hystophages of genera Coleps and Ophryoglena (76 % of the total abundance of ciliates in C. demersum), which consume decomposing plant tissues and even being predators. Probably, the degradation processes are more intensive in the C. demersum zone. In contrast, in Lake Raifskoe, located close to Lake Beloe, the predators are found only in plankton from macrophyte zone (Bykova, Zharikov, 2009). The reason of such differences is not obvious.
As a result of PCA analysis based on stand density index for all three groups of plankton from macrophyte association of three various zones (N. lutea, C. demersum and S. sagittifolia), we selected 2 groups which included species from phytoplankton, protozooplankton and zooplankton, corresponding to the first two principal components (Tabl 3). The selected two principal components describe more than 80 % of variability of structure of community. Probable, grouping factors for PCA axis were trophical preferences of protozooplankton and zooplankton depending on size.
The first principal component (61.57 % of variance explained of structure of community) contained colonial species of phytoplankton: Dinobrion divergens Imgh., Aulacoseira subarcticaca (O. Müller) Hawoath, Fragilaria virescens Ralfs, Eudorina cylindrica Korsch., Pediastrum duplex Meyen.; small copepods: Metacyclops gracilis gracilis (Lilljeborg, 1853) and cladocerans: Ceriodaphnia reticulate (Jurine, 1820), C. pulchella Sars, 1862, Alona rectangula Sars, 1862 (Fig. 4). This combination is explained by the fact that the large-sized colonial algae are more protected from the grazing by small zooplankton, which prefers protozoans from the same group: C. hirtus, C. hirtus viridis Ehrenberg, 1831, Furgasonia trichocystis (Stokes, 1894), Lembadion bullinum Perty, 1852, Strobilidium caudatum (Fromentel, 1876).
Table 3: Result of the Principal Components Analysis (PCA) for planktonic species, their interset correlation coefficients (r) with PCA axes, eigenvalue and the percentage of variance explained by the first two components for planktonic community in the Lake Beloe in July 2006. Only species with |r| > 0.9 are presented.
Species Abbreviation PCA Axis 1 PCA Axis 2
Phytoplankton
Microcystis pulverea (Wood) Forti emend. Elenk. aMp -0.178 0.984
Aulacoseira subarctica (Müller) Haworth aAsu 0.971 -0.239
Crucigenia tetrapedia (Kirchner) W. et G. S. West aCte -0.178 0.984
Dinobryon divergens Imhof aDd -0.995 -0.096
Eudorina cylindrica Korshikov aEcy 0.941 -0.338
Fragilaria crotonensis Kitton aFcr -0.084 -0.996
Fragilaria virescens Ralfs aFvi 0.941 -0.338
Gomphonema parvulum Kützing aGpa 0.303 -0.953
Kephyroin moniliferum (Schmid) Bourrelly aKm -0.178 0.984
Pandorina morum (Müller) Bory aPmo 0.999 -0.019
Pediastrum duplex Meyen aPdu 0.999 0.027
Scenedesmus denticulatus Lagerheim aSde -0.178 0.984
Scenedesmus armatus Chodat aSar -0.134 -0.991
Trachelomonas volvocina Ehrenberg aTvo -0.283 -0.959
Protozooplankton
Coleps hirtus (Muller) Nitzsch cChi 0.988 -0.153
Coleps hirtus viridis Ehrenberg cChv 0.957 -0.289
Furgasonia trichocystis (Stokes) cFtr 0.956 -0.292
Lembadion bullinum Perty cLbu 0.941 -0.338
Limnostrombidium viride (Stein) cLvi -0.178 0.984
Oxytricha sp. cOse -0.178 0.984
Pelagostrombidium fallax (Zach.) cPel -0.178 0.984
Stentor roesili Ehrenberg cSroe -0.178 0.984
Strobilidium caudatum (Fromentel) cScau -0.982 -0.188
Zooplankton
Asplanchna priodonta Gosse zApr -0.178 0.984
Alona rectangula Sars zAre 0.941 -0.338
Alona intermedia Sars zAin -0.263 -0.965
Ceriodaphnia pulchella Sars zCpu 0.991 -0.131
Ceriodaphnia reticulata (Jurine) zCre -0.999 -0.044
Daphnia cucullata Sars zDcu -0.178 0.984
Eucyclops macruroides (Lilljeborg) zEma -0.178 0.984
Mesocyclops leuckarti (Claus) zMle 0.284 0.959
Microcyclops gracilis (Lilljeborg) zMgr 0.941 -0.338
Sida crystallina (Müller) zScr 0.117 0.993
Eigenvalue 3.16 1.27
Variance explained, % 61.57 24.75
5.0-
2.5-
c\i
V)
<
O CL
1.0 0.5-
zDcu aKm QzScr 0 zCpuO
cScazApr 0 acLvP-cPel
cLb
zoo
-0.54
, zAre cChi ¡il OzMgr
-1.5
-1.0
-0.5
0.0-
4
rf)aSde
M
-2.5-
aDd
'zEm'a^' zMle O
S. sagittifolia N. lutea
aGpa
aTvo
phyto aPdu
C. demersum
-2.5
-0.5
1.5 PCA Axis 1
3.5
5.5
Fig. 4. Principal component analysis biplot of ordination between planktonic community and different biotopes of Lake Beloe in July 200(3. Plot of centroids (mean) of clouds distributions of the plankton community and some plankton species (species abbreviations are ginen in Table 3) in the space oo the first and second PCA axis; ± 95 % confidence interval. Grey circles - species most correlated (|r| > 0.9) with the first principal component, open circles - with the second principal component. PHYTO - phytoplankton, CIL - protozooplankton, ZOO -zooplankton
The second principal component (24.75 % of variance explained of structure of community) included small-sized solitary algae or small-sized colonial algae: M. pulverea, Kephyrion moniliferum (Schmid) Bourrelly, Gomphonema parvulum Kütz. var. parvulum, Trachelomonas volvocina Ehr., Crucigenia tetrapedia (Kirchn.) W. et G.S. West, Scenedesmus armatus Chrod. var. armatus, S. denticulatus Lagerh. var. linearis Hansg (Fig. 4). The listed above forms are bad food for the large forms of zooplankton also included to the same group: Asplanchna priodonta Gosse, 1850, Sida crystallina crystallina (O.F. Müller, 1776), Daphnia cucullata Sars, 1862, Eucyclops macrurus (Sars G.O., 1963), Mesocyclops leuckarti (Claus, 1857). Algophages and non-selective omnivorous ciliates were also in the same group: St. roeseli Ehrb., 1835, Oxytricha sp., Limnostrombidium viride (Stein, 1867), Pelagostrombidium fallax (Zach., 1895).
They were associated mainly with a community of S. sagittifolia and able to consume fine phytoplankton. Obviously, zooplankton in both cases prefers to consume medium-sized algae and ciliates (Nurminen, Horppila, 2002; Gulati, DeMott, 1997 et al.)
Our study has demonstrated that plankton of macophyte zone is characterized by a high species diversity and peculiarity of all groups as compared with pelagic zone of Lake Beloe.
Maximum total abundance and biomass of plankton (phyto-, protozoo-, and zooplankton) were registered in the zone of S. sagittifolia, maximum number of species was registered in the zone of C. demersum. However maximums of different plankton groups were registered in different zones: phytoplankton and ciliates - in submerged rooted hydrophytes (C. demersum, P. angustifolius); zooplankton - in zone of low-grasses helophytes (S. sagittifolia). Minimum
abundance, biomass and Shannon index is registered in the zone of plants with floating leaves (N. lutea) because of inhibition by nupharin, shadowing and closeness to pelagic zone.
We have not found any strong differences in the species composition of zoo- and phytoplankton between littoral zones covered by different macrophytes. However there were differences between the pelagic and littoral plankton: the absence of Cyanophyta in pelagic plankton; higher percentage of rotifers in pelagic zone as compared with littoral zooplankton; the presence of predaceous ciliates as a part of pelagic community, and the presence of hystohpages as a part of the littoral plankton community.
The peculiarity of our study is finding specific character of planktonic community organisms (protozoo-, zoo- and phytoplankton) in phytal zone of Lake Beloe, its comparing with pelagic complex of organisms and determining of its contributing factors.
Conclusion
Phytophilous flora and fauna play a significant role in species diversity development
References
in planktonic community of the lake, and communities of planktonic organisms forming in various ecotopes are characterized by high species diversity. Differences in components of planktonic community developing in the pelagic part of the lake and in individual macrophyte species are more significant than differences between macrovegetation plankton communities. Reaction of different planktonic community groups (phyto-, zoo-, ciliaplankton) to conditions in different ecotopes is similar in spite of peculiar properties of their biology and organization.
Acknowledgments
We express our deep gratitude to Gorshkov Yu.A., the director of the Volzhsko-Kamskiy Biosphere Natural State Reserve, for his assistance in organizing and carrying out works on the territory of the Biosphere Reserve. We thank V.M. Zhdanova for help in translating the manuscript and for valuable advice.
This work was supported by the Russian Foundation for Basic Research (project № 15-3450235).
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