Seasonal and annual population dynamics of

Fundam. Appl. Limnol., Arch. Hydrobiol. Stuttgart, February 2010

Vol. 176/2, 133–143

Article

Seasonal and annual population dynamics of ciliates in a shallow eutrophic lake Priit Zingel 1, 2 and Tiina Nõges 1 With 4 figures and 4 tables Abstract: Seasonal population dynamics and community composition of planktonic ciliates were studied for over

a decade in a naturally eutrophic shallow lake, Lake Võrtsjärv, which has a large open surface area (270 km2 on average) and highly turbid water (Secchi depth < 1 m). Our aim was to follow the seasonal and annual succession of planktonic ciliates and to analyse the factors controlling their development. Study material was collected from January 1995 to December 2007. The ciliate biomass was relatively high, accounting for more than 60 % of the total zooplankton biomass. We found a recurrent pattern in ciliate seasonal dynamics. Abundance peaked in spring (May) and reached its maximum in late summer (July, August). Large sized nanovorous oligotrichs dominated in spring. The summer peak was made up of small scuticociliates and oligotrichs, feeding mainly on picoplankton. A minor ciliate peak was also found in autumn (October); during this period when the community was dominated by species feeding on both pico- and nanoplankton. The highest biomass values were not always coupled with the peak abundances, but with the occurrence of large (Ø > 300 µm) gymnostomes. There was a positive correlation between ciliates and phyto- and bacterioplankton, implying that the ciliates were clearly bottom-up or food-controlled. This was further confirmed by the positive correlation between ciliates and metazooplankton. As both bacteria and phytoplankton are coupled with resuspension of lake sediments, the large fluctuations in water level influenced the ciliate community biomass annually. Key words: phytoplankton, bacterioplankton, turbid water, lake sediments, ciliate seasonal dynamics.

Introduction Ciliates are unicellular eukaryotes, which can be found in almost every aquatic environment. They have an important role in both freshwater and marine food webs, although their significance in pelagic food chains has been fully recognized only during recent decades. There is clear evidence that planktonic ciliates are an important food resource for large metazooplankton (e.g. Dolan & Coats 1991, Gifford 1991). The clearance rates of suspension-feeding zooplankton for ciliates are higher than for most phytoplankton. In

laboratory studies, protozoan components in the diet appear to enhance growth and survival during certain life-history stages or to enhance fecundity (Stoecker & Capuzzo 1990). It has been shown that metazooplankters suppress ciliates through predation and interference competition (Wickham & Gilbert 1991, Wickham & Gilbert 1993), while ciliates can consume sizeable proportions of bacterio- and phytoplankton production. Therefore, metazooplankton predation on ciliates can be an important trophic link between picoand nanoplankton and metazoans. In addition to their role in energy transfer to higher trophic levels, ciliated

Authors’ addresses: 1

Centre for Limnology, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Rannu, 61101 Tartumaa, Estonia. 2 Institute of Veterinary Medicine and Animal Sciences, Estonian University of Life Sciences, 1 Kreutzwaldi St., 51015 Tartu, Estonia. e-mail: pz [email protected] © 2010 E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, Germany DOI: 10.1127/1863-9135/2010/0176-0133 eschweizerbart_xxx

www.schweizerbart.de 1863-9135/10/0176-0133 $ 2.75

134

Priit Zingel and Tiina Nõges

protozoa act in the bio-geochemical cycling of phosphorus and nitrogen and can increase the availability of nutrients for phytoplankton growth (Buechler & Dillon 1974, Berman et al. 1987). It is well known that ciliate communities are very dynamic, and their community structure may respond quickly to changing physical, chemical and biological conditions in the environment (e.g. Carrick & Fahnenstiel 1990, Laybourn-Parry et al. 1990, Carrias et al. 1994, James et al. 1995, Mayer et al. 1997, Biyu 2000, Wiackowski et al. 2001, Jezbera et al. 2003). Few studies, however, have paid attention to the annual dynamics of planktonic ciliates. The aim of this study was to describe the community structure, abundance and seasonality of planktonic ciliated protozoa in a shallow eutrophic lake over thirteen consecutive years.

Material and methods Lake Võrtsjärv is a large (270 km2) and shallow (mean depth 2.8 m, maximum depth 6 m) eutrophic lake situated in the Central Estonian depression, which is of preglacial origin. The water temperature reaches its maximum in July (20.1 °C on average). The ice cover lasts from November to April (135 days on average). Homothermy prevails in Võrtsjärv throughout the year (Nõges et al. 1998). The water is slightly alkaline, the monthly mean pH ranging from 7.6 to 8.5, salinity from 227 to 370 mg l–1, and the concentrations of chlorides and sulphates from 9 to 14 mg l–1 and from 17 to 21 mg l–1, respectively. Average chemical and biochemical oxygen demand (COD by K2MnO4 method and BOD7) are 11 and 3.8 mg O l–1, respectively. The average total phosphorus concentration (Ptot) is 54 µg l–1, total nitrogen concentration (Ntot) 1.6 mg l–1, and the mean Secchi depth 1.1 m (Nõges et al. 1998). During the vegetation period, Secchi depth does not usually exceed 1 m. Algal blooms are a common phenomenon in Võrtsjärv. Besides this, the shallowness of the lake and the wave-induced resuspension of bottom sediments contribute to the formation of a high seston concentration and high turbidity during summer. Most of the organic compounds in the lake are of autochthonous character (Nõges et al. 1998). Ciliate samples were collected using either Moltchanov’s sampler or a Ruttner sampler. The samples were collected weekly in 1995, biweekly in 1996–2000 and monthly in 2001– 2007 at a station close to the deepest area of Võrtsjärv. Integrated samples were used (water taken from the whole water column with an interval of 0.5 m and mixed in one large tank) and 250 ml subsamples were preserved and fixed with acidified Lugol’s solution. Ciliate biomass and community composition were determined using the Utermöhl (1958) technique. The samples were stored at 4 °C in the dark. Volumes of 10–100 ml were allowed to settle for at least 24 h in plankton chambers. Ciliates were enumerated and identified with an inverted microscope (Wild Heerbrug M40 and Nikon diaphot-TMD) at × 200–600 magnification. The entire content of each Utermöhl chamber was surveyed; if the total tally in the counting chamber was < 150 organisms, an additional subsample was counted. The first 20 measurable specimens encountered for each taxon were measured. The biovolume of each taxon was estimated

by assuming geometric shapes. Specific gravity was assumed to be 1.0 g ml–1 (Finlay 1982), and biomass was expressed as wet weight (WW). Ciliates were identified by consulting several works (Kahl 1930–1935, Foissner & Berger 1996, Foissner et al. 1999). The taxonomy followed the scheme of Corliss (1979). Many of the ciliates found were identified only to the genus level. More accurate identification is not usually possible from Lugol-fixed samples. On several occasions, therefore, we also used additional live subsamples to aid identification, as recommended in Foissner & Berger (1996). Silver impregnation techniques were also used to identify some species (Foissner et al. 1999). The ciliates were divided into five ecological groups using data gathered during several feeding experiments (e.g. Kisand & Zingel 2000, Agasild et al. 2007, Zingel et al. 2007, Zingel & Nõges 2008). The ability of the ciliates to graze on picoplankton was determined by in situ feeding experiments using fluorescently labelled bacteria (heat-killed and DTAF-stained according to the protocol of Sherr & Sherr (1993)) or fluorescent microspheres of 0.5 µm diameter (Fluoresbrite, Polysciences Inc.). Fluorescent microspheres of 3, 6, and 24 µm diameter (Duke Scientific Corporation) were used to study ciliate grazing on unicellular phytoplankton. Algivory was also deduced by inspecting the food vacuoles in ciliate cells in sedimented samples. Data from the literature were also considered (Foissner et al. 1991, 1992, 1994, 1995). We used following ecological groups: bacterivores (picovores), herbivores (nanovores), bacteri-herbivores (pico-nanovores), predators (consumers of ciliates and small metazooplankters) and omnivores. We are fully aware that this division is not perfect and not entirely comprehensive, but the most common ciliate species forming most of the biomass and abundance in Võrtsjärv could be divided quite reasonably in that way. The abundance of bacteria (direct count) was determined under an epifluorescence microscope (magnification 1000×) as in Tulonen (1993). For metazooplankton samples, 10 l integrated lake water was filtrated through a 48 µm plankton net and concentrated to about 100 ml. The samples were fixed with acidified Lugol’s solution. Triplicate subsamples (2.5 or 5 ml) of each metazooplankton sample were counted under a binocular microscope in a chamber (dimensions 13 × 6 cm, capacity 8 ml) at 32 and 56× magnifications. Phytoplankton species composition and biomass were also analyzed using the Utermöhl (1958) technique. The program STATISTICA for Windows version 6.0 was used for statistical analyses. Spearman’s correlation coefficients were used to determine the relationships between annual average values of ciliates and other plankton components. To avoid erroneous results due to non-normal distribution of data, all values except water level were ln-transformed before the Pearson product moment correlation analysis. To identify patterns in our multivariate dataset, we applied the Factor Analysis option of the Multivariate Exploratory Technique module of STATISTICA, which yields a two-factor solution of principal component extraction. The varimax normalized method was used for factor rotation.

Results The ciliate community composition

During the study period oligotrichs, haptorids, scuticociliates, prostomatids and peritrichs dominated the eschweizerbart_xxx

Seasonal succession of ciliates

135

Fig. 1. Seasonality of Lake Võrtsjärv planktonic ciliates during 1995–2007. Seasonal changes in relative importance of main taxo-

nomic orders (A). Seasonal changes in number of taxa found. Where taxonomic resolution achieved only the genus level we used genus as a representative of one taxon (B). Mean ciliate abundance and biomass (C).

community of ciliates, usually constituting over 90 % of the total abundance. Oligotrichs were always the most numerous, accounting for 27–78 % of the total monthly average ciliate abundance (Fig. 1A). The most common oligotrichs were Rimostrombidium spp., Limnostrombidium spp., Pelagostrombidium spp., Halteria spp., Codonella cratera and Tintinnidium fluviatile. All these species were present throughout the year with the exception of Halteria, which occurred only during summer. Oligotrichs were followed in numbers by prostomatids (11–25 % of the total monthly average ciliate abundance), haptorids (4–34 %) and scuticociliates (0.3–22 %). The most common prostomatids were Urotricha spp., Balanion planktonicum, Coleps hirtus and Coleps spetai. Mesodinium spp., Dileptus sp., Askenasia volvox and Didinium spp. were the most common haptorids, but they were present sporadically – only Mesodinium spp. could be found in all seasons. The most important scuticociliates were Uronema sp. and Cyclidium sp., which were especially numerous during the summers. Peritrichs were present only dureschweizerbart_xxx

ing warm seasons in Võrtsjärv – they were never found in winter. The most common peritrichs were species from the genera Vorticella and Epistylis. The other ciliate orders found in Võrtsjärv were Colpodida, Nassulida, Heterotrichida, Hymenostomatida, Hypotrichida, Pleutostomatida and Suctorida. Their abundance was usually low and even taken together they did not exceed 10 % of the total ciliate abundance. The greatest species diversity always occurred in June (Fig. 1B). Altogether, we found 73 taxa of ciliates in Võrtsjärv; a list is given in Table 1. Seasonal and annual dynamics of ciliates

The seasonal dynamics of ciliates followed an established pattern throughout the study period. In winter (January-March) the community of ciliates was dominated by large (Ø > 50 µm) oligotrichs, prostomatids and haptorids. During this period the number and biomass of ciliates was low (Fig. 1C). This situation lasted until the breaking up of the ice, when the abundance of ciliates started to rise rapidly. This peak

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Table 1. Ciliate species found in Lake Võrtsjärv in 1995–2007. B = bacterivores (picovores), H = herbivores (nanovores), BH = bacteri-herbivores (pico-nanovores), P = predators (consumers of ciliates and small metazooplankters), O = omnivores.

Colpodida Bursaridium pseudobursaria Fauré-Fremiet, 1924 Colpoda steini Maupas, 1883 Cyrtolophosis mucicola Stokes, 1885 Haptorida Cyclotrichium limneticum Kahl, 1932 Didinium nasutum (Mueller, 1773) Stein, 1859 Didinium sp. Monodinium balbiani Fabre-Domergue, 1888 Mesodinium pulex Claparéde & Lachmann, 1858 Mesodinium sp. Askenasia volvox Claparéde & Lachmann, 1859 Lacrymaria sp. Dileptus sp. Paradileptus elephantinus Kahl, 1931 Pelagodileptus trachelioides Zacharias, 1894 Actinobolina radians Stein, 1852 Actinobolina sp. Ilonema sp. Heterotrichida Stentor amethystinus Leidy, 1880 Stentor roeselii Ehrenberg, 1835 Spirostomum sp. Hymenostomatida Frontonia sp. Lembadion magnum (Stokes, 1887) Kahl,1931 Paramecium sp. Disematostoma tetraedricum Fauré-Fremiet, 1924 Scuticociliatida Cyclidium sp. 1 Cyclidium sp. 2 Calyptotricha lanuginosa Penard, 1922 Uronema sp. Hypotrichida Oxytricha sp. Euplotes sp. Stylonychia mytilus Ehrenberg, 1838 Uroleptus piscis Müller, 1773 Stichotricha aculeata Wrzesniowski, 1866 Nassulida Nassula sp.

H B B O P P P H H H P P P P P P P BH O BH O O BH H B B BH B O O O O BH H

Oligotrichida Rimostrombidium lacustris Foissner, Skogstad & Pratt, 1988 Rimostrombidium sp. 1 Rimostrombidium sp. 2 Rimostrombidium humile Penard, 1922 Limnostrombidium viride Stein, 1867 Limnostrombidium sp. Pelagostrombidium fallax Krainer, 1991 Pelagostrombidium sp. Halteria bifurcata Tamar, 1968 Halteria grandinella (Müller, 1773) Dujardin, 1841 Tintinnidium fluviatile Stein, 1833 Tintinnidium pusillum Entz, 1909 Tintinnopsis cylindrata Koffoid & Campbell, 1929 Tintinnopsis tubulosa Levander, 1894 Tintinnopsis sp. Codonella cratera Leidy, 1877 Peritrichida Vorticella natans Fauré-Fremiet, 1924 Vorticella sp. 1 Vorticella sp. 2 Opercularia sp. Scyphidia sp. Carchesium pectinatum (Zacharias, 1897) Kahl, 1935 Vaginicola ingenita Müller, 1786 Epistylis anastatica (Linnaeus, 1767) Ehrenberg, 1830 Epistylis procumbens Zacharias, 1897 Lagenophrys vaginicola Stein, 1852 Ophrydium versatile Müller, 1786 Pleutostomatida Litonotus sp. Loxophyllum sp. Prostomatida Urotricha furcata Schewiakoff, 1892 Urotricha farcta Claparéde & Lachmann, 1859 Urotricha globosa Schewiakoff, 1892 Urotricha pelagica Kahl, 1935 Balanion planctonicum Foissner, Berger & Kohmann, 1994 Coleps hirtus Müller, 1786 Coleps spetai Foissner, 1984 Coleps sp. Suctorida Podophrya sp. Sphaerophrya magna Maupas, 1881

was mostly due to large herbivores (mostly Pelagostrombidium spp. Codonella cratera and Tintinnidium fluviatile) (Fig. 2). The maximum numbers in spring were usually achieved in May, to be followed by a fast decrease in June. The second large peak of ciliates occurred in late July or early August, at the time of maximum annual abundance. In contrast to spring, the community of

H B BH BH BH H BH H B B H BH H H H H BH B B B B B B B B B BH P P BH BH BH BH BH O O O P P

ciliates during this period was dominated by small bacterivorous species such as Rimostrombidium sp., Halteria sp., Uronema spp. and Cyclidium spp. Since they are mostly very small species, they do not have a very marked impact on the total ciliate biomass. The peritrichs also achieved their maximum numbers in this period. During autumn, the abundance of ciliates peaked again in October. In this period the community eschweizerbart_xxx


137

Fig. 2. Seasonal changes in relative

importance of different trophic ciliate groups in Lake Võrtsjärv as a percentage of abundance during 1995–2007.

Table 2. Correlation coefficients (Spearman R, p < 0.01) between yearly average cell density and biomass of planktonic ciliates, and water level, bacterial abundance, chlorophyll-a, phytoplankton biomass and metazooplankton biomass in Lake Võrtsjärv. NS = not significant.

Water level Bacterial abundance Chl-a Phytoplankton biomass Metazooplankton biomass

Ciliate abundance

Ciliate biomass

–0.28NS 0.71 0.90 0.24NS 0.10NS

–0.58 0.62 0.90 0.52 –0.05NS

was dominated by bacteri-herbivorous species (Balanion planktonicum, Urotricha globosa, Limnostrombidium viride, Tintinnidium pusillum). The abundance of bacterivores decreased and peritrichs disappeared from the lake’s plankton. Ciliate abundance and biomass fluctuated annually (Fig. 1A) and the annual average values correlated significantly (p < 0.01) with water level, bacterial numbers, chlorophyll-a and phytoplankton biomass (Table 2). Maximum ciliate abundance (284.7 cells ml–1) and biomass (15.4 µg ml–1) were found in August 2006; the respective minimum values were found in February 1995 (0.8 cells ml–1 and 0.02 µg ml–1). Mean abundance was (52.3 ± SE 4.8 cells ml–1) and mean biomass (1.8 ± SE 0.2 µg ml–1). The maximum biomasses usually occurred during the spring and summer abundance peaks. However, there were exceptions to this rule; in some years the highest biomass values were accompanied with peaks of large (Ø > 500 µm) haptorids (e.g. Paradileptus elephantinus, Pelagodileptus trachelioides). Their abundance was not high and their occurrence was very sporadic, but their contribution to the total biomass was significant owing to their large eschweizerbart_xxx

size. For example, in 1996 the maximum biomass (7.4 mg l–1) was achieved in October, and consisted to 97 % of the large haptorid species Pelagodileptus and Paradileptus. The importance of ciliate orders varied from year to year. The most stable group was haptorids, accounting for 14–20 % of total annual abundance; the most variable was scuticociliates, accounting for 4–28 %. Oligotrichs, prostomatids and peritrichs accounted respectively for 32–66 %, 5–27 % and 2–10 %. Meanwhile, the ecological groups showed much more stable dynamics, the differences between the minimum and maximum percentages of total abundance varying between 1.1 (bacterivores) and 1.7 (omnivores) times. Ciliates formed 11.2–99.9 % of the total zooplankton biomass (metazooplankton + ciliates), the average value being 66.3 % (Fig. 3). The highest percentages were found in April (average 85.1 %) and the lowest in June (average 45.7 %). Factors determining ciliate distribution patterns

Factor analyses of the whole dataset showed that all ciliate groups combined in the first factor positively with total metazooplankton abundance and biomass (Table 3). Correlation analysis also revealed that the metazooplankton was positively related to the ciliates (Table 4). Rotifers were the only metazooplankton group that showed a negative correlation with ciliates. In the whole dataset, water transparency had a high weight in the second factor, combining inversely with phytoplankton biomass and Chl-a, but not with ciliates. Correlation analyses showed that most ciliate groups correlated similarly (Table 4). Herbivores were the only group that showed a weak positive correlation with lake water level and a negative correlation with cladoceran abundance; they did not correlate signifi-

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Fig. 3. Changes in ratio between ciliates and metazooplankton in Lake Võrtsjärv as a percentage of total zooplankton biomass.

cantly with total phosphorus. Bacteri-herbivores correlated positively with cladocerans. In the spring dataset, the water transparency related in the first factor inversely to all ciliate groups, phytoplankton, Chl-a and metazooplankton. The same trend was revealed by correlation analysis (Fig. 4). In summer, the water transparency and water level combined inversely with bacterivores, bacteri-herbivores and predators in the first factor. Bacteri-herbivores and herbivores correlated positively with Chl-a (Fig. 4). In autumn, all ciliate groups combined positively with Chl-a in the first factor. Correlation analyses confirmed that trend. In addition, bacterivores and omnivores correlated positively with metazooplankton biomass. In winter, ciliates densities did not correlate significantly to any of the factor studied (Fig. 4).

Discussion The abundance of planktonic ciliates recorded in Võrtsjärv corresponds to the range reported for eutrophic subtropical lakes (mean 55.5 cells ml–1, Beaver & Crisman 1982) and is higher than in many eutrophic temperate lakes (mean < 10 cells ml–1, Laybourn-Parry 1992). Ciliates are usually strongly suppressed by metazooplankton communities (Jürgens et al. 1999,

Hansen 2000). However, this might not be the case in shallow and turbid environments with high abundances of filamentous algae and strong resuspension. We speculate that in turbid environments with a highly abundant filamentous phytoplankton community, resuspended particles disturb the grazing by metazooplankton (Nõges et al. 1998). This assumption is corroborated by our short-term grazing experiments with natural assemblages of planktonic ciliates labelled with fluorescent microparticles (Agasild et al. 2010) indicating low crustacean predation rates in L. Võrtsjärv (0.2–14.3 % on the 15–40 µm sized ciliate standing stock d–1). The ciliate genera found in this study are typical of temperate lakes. In Võrtsjärv, the community numbers were dominated by oligotrichs, haptorids, scuticociliates and prostomatids. All these groups are often reported as common components of lacustrine protozooplankton (Mamaeva 1976, Pace & Orcutt 1981, Hecky & Kling 1981, Beaver & Crisman 1982, Carrick & Fahnenstiel 1990, Laybourn-Parry et al. 1990, Müller et al. 1991, James et al. 1995). Our analyses showed that in Võrtsjärv, ciliates were mainly bottom-up controlled. In spring, both ciliates and crustacean metazooplankters depended on phytoplankton and were positively related. Rotifer densities correlated negatively with ciliates, indicating probable eschweizerbart_xxx

Factors

eschweizerbart_xxx

F1 49.9 % 0.18 –0.30 0.93 0.95 0.89 0.87 0.88 0.87 0.83 0.44 0.44 0.73 0.68 0.39 –0.13 –0.32 0.27 –0.39 0.14

F2 13.9 % –0.35 –0.78 0.22 0.22 0.30 0.31 –0.16 0.23 0.20 0.76 0.74 0.08 0.46 0.39 0.77 –0.76 0.38 –0.57 0.55

F1 54.2 % 0.34 –0.70 0.92 0.93 0.92 0.93 0.92 0.82 0.72 0.84 0.87 0.86 0.87 0.28 –0.04 –0.63 0.02 –0.52 0.47

Spring F2 11.0 % –0.08 –0.02 0.24 0.19 0.11 0.15 0.21 0.30 0.30 –0.05 0.02 –0.24 –0.20 0.76 0.83 –0.50 0.15 –0.50 –0.35

F1 32.0 % –0.61 –0.67 0.83 0.89 0.77 0.76 0.50 0.72 0.56 0.48 0.52 0.22 –0.22 –0.18 –0.44 –0.17 0.43 0.13 0.07

F2 16.2 % 0.42 0.21 0.19 0.17 –0.01 0.42 0.34 0.13 0.20 –0.35 0.23 0.82 –0.27 –0.77 –0.69 0.60 –0.07 0.29 –0.70

Summer F1 36.6 % –0.30 –0.26 0.90 0.97 0.79 0.80 0.87 0.83 0.83 0.30 0.60 0.38 0.29 0.35 –0.12 0.16 0.32 0.03 0.28

F2 14.1 % –0.51 –0.69 0.04 0.11 0.13 0.04 –0.04 0.08 0.35 0.57 0.31 0.07 0.48 0.13 0.59 –0.73 –0.19 0.38 0.81

Autumn F1

31.3 % –0.50 –0.11 0.93 0.98 0.96 0.85 0.72 0.79 0.90 0.17 0.14 –0.08 –0.07 –0.07 –0.14 –0.19 0.00 0.14 0.07

F2 18.5 % –0.07 –0.66 0.09 0.01 0.05 0.19 –0.22 0.05 0.09 0.87 0.90 0.56 0.56 0.03 0.39 –0.39 0.53 –0.54 –0.05

Winter

Percentages show for how much variability the corresponding factor accounts. The highest factor scores (> 0.6 and < –0.6) are marked in bold. Ciliate functional groups are presented as abundance; MZP = metazooplankton.

Variability described Water level Secchi depth Ciliate biomass Ciliate abundance Bacterivores Bacteri-herbivores Herbivores Predators Omnivores Phytoplankton biomass Chlorophyll-a MZP abundance MZP biomass Copepod abundance Cladocers abundance Rotifer abundance Bacterial abundance Total nitrogen Total phosphorus

Whole year

August), autumn (September–November) and winter (December–February).

Table 3. Factor scores of the selected plankton and lake indices in the whole valid lake data set for factor analysis, and in different seasons: spring (March–April), summer (June–


139

140


Fig. 4. Pearson correlation coefficients (r) of different functional ciliate groups with metazooplankton biomass (= MZP), chloro-

phyll-a (= CHL) and Secchi depth (= Secchi) in different seasons: spring (March–April), summer (June–August), autumn (September–November) and winter (December–February). All values are ln-transformed. r values > 0.3 and < –0.3 (see line in the figures) are significant at least at p < 0.05. Table 4. Pearson product moment correlation coefficients among variables, all ln-transformed except water level. P < 0.05.

NS = non-significant. PP = phytoplankton, Chl-a = Chlorophyll-a, MZP = metazooplankton, N tot = total nitrogen, P tot = total phosphorus, bm = biomass, ab = abundance. Ciliate and metazooplankton groups are presented as abundance.

Water level Secchi depth PP bm CHL-a MZP ab MZP bm Copepods Cladocers Rotifers Bacterial ab N tot P tot

Ciliates bm

Ciliates ab

Bacterivores

Bacteriherbivores

Herbivores

Predators

Omnivores

NS –0.44 0.56 0.56 0.59 0.64 0.48 NS –0.47 0.34 –0.43 0.25

NS –0.44 0.56 0.54 0.64 0.69 0.46 NS –0.49 0.32 –0.48 0.29

NS –0.48 0.59 0.55 0.62 0.70 0.49 NS –0.53 0.34 –0.52 0.32

NS –0.48 0.60 0.62 0.56 0.66 0.39 0.17 –0.49 0.27 –0.49 0.34

0.16 –0.18 0.24 0.26 0.54 0.46 0.29 –0.17 –0.19 0.20 –0.18 NS

NS –0.38 0.50 0.50 0.56 0.64 0.45 NS –0.47 0.26 –0.49 0.25

NS –0.410 0.50 0.51 0.52 0.55 0.43 NS –0.41 0.36 –0.36 0.24

food competition between these two groups. Lower Chl-a concentrations and accordingly also fewer ciliates and crustancean zooplankton were associated with greater water transparency (Table 3, Fig. 4). In summer, the bacterivores, bacteri-herbivores and predators were negatively related to water level and water transparency. This indicates that the microbial loop grows stronger in a more shallow and turbid environment. It

is known that during years with low water level the resuspension of sediments is more intensive and a large amount of nutrients may be released from the sediment pore-water. This leads to a rapid increase of Chl-a and phytoplankton biomass (Nõges & Nõges 1998, Kisand & Nõges 2004). In Võrtsjärv, water level fluctuations can be considered to be among the most important environmental factors shaping both the phytoplankton eschweizerbart_xxx


and the bacterial community (Nõges & Kisand 1999). Bacteria become the most important food item for zooplankton during summer when the amount of small edible algae is low (Nõges et al. 1998). This implies that the benthic detrital food chain and the microbial loop are responsible for most of the transformation of organic matter (Nõges et al. 2004). This is reflected in the high bacterial production (70 % of primary production) (Nõges et al. 2004). On the basis of our grazing experiments from the year 2000 (Zingel et al. 2007), we conclude that zooplankton grazing rates on both bacteria and phytoplankton in Võrtsjärv are low. On average, only 0.1 % and 1.0 % of the standing stocks of bacteria and ingestible phytoplankton, respectively, were grazed by metazooplankton daily. The main grazers of pico- and nanoplankton were ciliates. In summer, herbivorous and bacteri-herbivorous ciliates showed a negative correlation with water transparency and a positive one with Chl-a, indicating bottom-up control (Fig. 4, Table 3). Most ciliate groups (the only exception being herbivores) showed non-significant negative correlations with metazooplankton biomass. As this relationship was positive during spring and autumn, it may still indicate some weak top-down regulation in summer (Fig. 4). Considering the metazooplankton composition in Võrtsjärv, i.e., an abundant population of small rotifers (Keratella spp., Polyarthra spp., Anuraeopsis fissa, and Trichocerca spp.), small-bodied cladocerans (mainly Chydorus sphaericus), and cyclopoid copepods (Mesocyclops spp.), a high grazing pressure on ciliates would be unlikely. However, our grazing studies still indicate that metazooplankton has some influence on the ciliate community: an increase in the feeding rate of metazooplankton results in a decrease in that of ciliates (Zingel et al. 2006). During autumn, ciliates were again clearly bottomup controlled, relating positively to Chl-a. Several authors (e.g. Beaver & Crisman 1982) have suggested that limiting food resources rather than metazoan grazing control the community composition and abundance of ciliates. This also seems to be the case in Võrtsjärv, where ciliates were clearly food-limited most of the time.

Conclusions Ciliate biomass and abundance fluctuated annually, but the seasonal dynamics and community structure followed a fixed pattern. Four distinct quarters were described: eschweizerbart_xxx

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I (January–March) low abundance, community is dominated by herbivores. II (April–June) spring peak, community is dominated by herbivores. III (July–September) summer peak, community is dominated by bacterivores. IV (October–December) autumn peak, community is dominated by bacteri-herbivores. There was a positive correlation between ciliates and phyto- and bacterioplankton, implying that the ciliates were clearly bottom-up or food-controlled. This was further confirmed by the positive correlation between ciliates and metazooplankton. As both bacteria and phytoplankton are coupled with resuspension of lake sediments, the large variations in water level also influenced the ciliate community biomass. Acknowledgements Funding for this research was provided by the Estonian Ministry of Education (SF 0170011508) and Estonian Science Foundation grants 4080, 5738 and 7600.

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Submitted: 5 March 2009; accepted: 9 March 2010.

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