Journal of Plankton Research Vol.20 no.8 pp. 1435-1448, 1998
Grazing on autotrophic and heterotrophic picoplankton by ciliates
isolated from Lake Kinneret, Israel
O.Hadas1, N.Malinsky-Rushansky1-2, R-Pinkas1 and T.E.Cappenberg3
Israel Oceanographic and Limnological Research, The YigalAllon Kinneret
Limnological Laboratory, PO Box 345, Tiberias 14102,2Department of Life
Sciences, Bar-Han University, Ramat-Gan, Israel and 3Centrefor Coastal and
Estuarine Ecology, Netherlands Institute of Ecology, 4401 EA Yerseke, The
Netherlands
1
Abstract. The rates of ingestion of three ciliates (Colpoda steinii, Cyclidium sp. and Stylonichia sp.)
on fluorescently labeled heterotrophic bacteria, picocyanobacteria (Synechococcus P, CN) and a
picoeukaryote isolated from Lake Kinneret were measured. Uptake values were 930, 35 and 1210
bacteria ciliate (cil)"1 h~' for Colpoda, Cyclidium and Stylonichia, respectively, depending on prey
concentrations. An increase in prey concentration resulted in a decrease in clearance rates from 405
to 32 nl cil~' h~'. Clearance rates of Colpoda fed on Synechococcus (P, CN) and on picoeukaryotes
ranged from 27 to 62 and from 3 to 7 nl cil"1 h~', respectively. Cyclidium, which is classified as a
picoplankton feeder, showed lower clearance rates when fed on Synechococcus P and bacteria.
Specific clearance (body volume cell"1 h~') for the three ciliates studied decreased when prey supply
increased, for all three food sources. Relating to body volume, Colpoda could manage successfully on
bacteria as its sole food source. It appears from our measurements that bacteria in Lake Kinneret are
abundant enough to sustain the carbon requirements of Colpoda.
Introduction
The role of protozoa [heterotrophic nanoflagellates (HNAN) and ciliates] in
structuring the food web in marine and freshwater ecosystems has been documented in many studies. Bacterivory has been found to be an important food
source for HNAN and ciliates (Fenchel, 1987; Sherr and Sherr, 1987; Sanders et
ai, 1989; Pace et al., 1990; Caron et ai, 1991). Abundances of >5 x 106 bacteria
ml-1 were considered as a sufficient carbon source to supply the nutritional
requirements of ciliates (Fenchel, 1980; Rivier et ai, 1985; Beaver and Crisman,
1989). Such concentrations are usually found in eutrophic waters and specific
environments, such as the chemocline-oxycline zone (Fenchel et al., 1990;
Zubkov etal., 1992).
Autotrophic picoplankton are a ubiquitous component of marine and freshwater environments, and may serve as a potential food source for ciliates (Stockner, 1988; Sherr et al., 1991; Weisse, 1993). Grazing rate measurements performed
in Vineyard Sound, USA, revealed removal rates by nanoplanktonic protists as
high as 54 and 75% of the cyanobacterial and heterotrophic bacterial assemblage,
respectively (Caron et al., 1988). In a eutrophic reservoir in Bohemia (Czech
Republic), picoplankton covered most of the carbon requirements of pelagic
ciliates (mainly oligotrichs), and were probably an important prey for metazoa
(Simek etal., 1995,1996).
In Lake Kinneret, ciliate abundance was maximal at the thermocline/oxycline
region in autumn when picocyanobacteria reached abundances of 6 x 105 cells
ml"1, with low contribution (-6%) to total phytoplankton standing stocks
© Oxford University Press
1435
OJiadas et al.
(Malinsky-Rushansky et al, 1995; Hadas and Berman, 1998). This may indicate
that natural populations of HNAN and ciliates in the lake control the bacteria
and autotrophic picoplankton populations through grazing (Sherr etal, 1991).
In the present study, we used grazing experiments to evaluate the ability of
Lake Kinneret protozoa to graze efficiently on bacteria and autotrophic
picoplankton.
Method
Isolates
Two picocyanobacteria, P and CN, identified as Synechococcus sp., and a
Chlorella-like picoeukaryote (Malinsky-Rushansky et al, 1995), with average
biovolumes of 0.5 and 4.2 um3, respectively, were isolated from Lake Kinneret
and grown on medium BG-11 (Stanier et al, 1971) at 20°C and irradiance of
~50 uE m~2 s"1. A rod-shaped bacterium (designated as Ti0), with an average
biovolume of 0.4 urn3, was isolated from the lake and grown on nutrient broth
(Difco) at 37°C. During late logarithmic growth phase, the cultures were
harvested and washed twice by centrifugation (Sorvall 5B, 10 000 r.p.m.). After
resuspension, the pellet was used as a food source for protozoa. In addition, the
bacteria were used for fluorescently labeled bacteria (FLB) preparation, according to the method of Sherr et al. (1987). Three ciliates, isolated from the lake, and
identified as Colpoda steinii (family Colpodidae, genus Colpoda), Stylonichia sp.
(family Oxytrichidae, genus Stylonichia) and Cyclidium sp. (family Cyclidiidae,
genus Cyclidium), were grown on S.C. medium (Moss, 1972). All ciliate cultures
were kept in the dark and fed T10 bacteria.
Biovolumes
Live individuals of protozoa from samples of different cultures were examined
microscopically. The linear dimensions of the organisms were determined from
their geometrical shape using appropriate equations. Biovolumes of Colpoda
and Cyclidium were calculated as prolate spheroids: V = (re/6) (W2/-), where V
is the volume, and W and L are the width and the length, respectively. Biovolumes of Stylonichia were calculated as V = W X L X T, where T is the thickness. Biovolumes of picoeukaryotes from preserved samples were calculated as
for coccoid cells, i.e. V = (4/3) (n r 3 ), where r is the radius. Bacteria and picocyanobacteria were calculated as rods (Table I). Cell volumes were transformed
to organic carbon, using conversion factors of 0.22 and 0.14 pg C unr 3 for
picoplankton and ciliates, respectively (Bratbak and Dundas, 1984; Putt and
Stoecker, 1989).
Grazing experiments
Protozoan cultures (1 ml) were transferred to a flask containing 200 ml S.C.
medium, and 2 ml yeast extract (2 mg ml'1) were added 48 h before the grazing
1436
Grazing on autotrophic and heterotrophic picoplankton
Table I. Morphometric properties of ciliates, bacteria and picophytoplankton isolated from Lake
Kinneret
Organism
Colpoda steinii
Cyclidium
Stylonichia
Bacterium T,o
Synechococcus P, CN
Picoeukaryote
50
34
30
105
50
50
Average length
Average width
(pm)
Average biovolume
(Mm3)
24.9 ± 4.2"
19.2 ± 12
118.2 ± 18.2
1.4 ±0.5
1.14 ±0.28
2 ± 0.16
14.8 ± 1.7
11.3 ±1.5
46.8 ± 11.4
0.6
0.75
2
2988.4 ± 1069.7
1311.2 ±346.2
56 927 ±15 716
0.4
0.5
4.2
'± standard deviation.
experiment. Before the beginning of the experiments, bacterial concentrations
were determined by DAPI staining (Porter and Feig, 1980), while autotrophic
picoplankton were counted using their autofluorescence. Labeled bacteria were
added to reach concentrations of 3-7% of total bacteria. Short-term uptake of
bacteria or autotrophic picoplankton by ciliates was measured after 0, 5,10, 20,
30, 40 and 60 min. At each time, a subsample of 9 ml was taken and fixed with
1 ml of a 1:1 (v/v) mixture of glutaraldehyde and paraformaldehyde (Tsuji and
Yanagita, 1981). The cell ingestion rate per sample was determined by counting
the number of FLB or autotrophic picoplankton within the protoplast of 100
protozoans using an epifluorescence microscope (Zeiss Axioscope). Filters used
were: (1) for bacteria (UV excitation G365, chromatic beam splitter FT395, longwave pass filter LP420), (2) for picocyanobacteria (green excitation filter 510-560,
chromatic beam splitter FT580, barrier filter LP590) and (3) for the picoeukaryotes (blue excitation filter G436, chromatic beam splitter FT510, barrier filter
LP520).
Counting procedure
Five milliliter portions of the time series subsamples were filtered through 0.8 |im
polycarbonate (Poretics) black filters stained with the fiuorochrome Primuline
according to Bloem et al. (1986). The number of FLB within one ciliate was
counted at X1000 magnification for Colpoda and Cyclidium or X400 for
Stylonichia. No staining of protozoa was necessary in grazing experiments using
Synechococcus and picoeukaryotes since their pigments and the contour of the
ciliate cells were clearly seen under the epifluorescence microscope. The FLB
ingestion rate was used to derive an average clearance rate of picoplankton [nl
ciliate (cil)"1 h"1] using the equation C = //picoplankton, where C is clearance rate,
/ is picoplankton ingested per ciliate per hour, and picoplankton is the concentration of picoplankton per nanoliter.
Population clearance (h"1) was the clearance rate by ciliates (nl ciH h"1) multiplied by the number of ciliates.
Specific clearance was expressed as the number of body volumes cleared per
ciliate per unit of time (h) (Sherr and Sherr, 1987).
1437
OJiadas et al.
Doubling times
Doubling times {dT) of ciliates were calculated from changes in the number of
cells during the experiment, based on exponential growth rates (u), calculated
from u = (In Ni/N0)/(Ti - TQ), where No and Ni are the ciliate numbers at the
beginning and the end of the experiments, and (Tx- To) is the duration of the
experiment. The doubling times were calculated as dT = In 2/u.
Doubling times of ciliates were also calculated from the grazing experiments,
using the organic carbon consumed (food particles cil"1 h"1) multiplied by the
organic carbon of the food particle. To convert the carbon consumed into potential doubling times, we used a gross growth efficiency of 50% (Fenchel, 1987;
Sherr era/., 1991).
Results
Colpoda steinii is capable of growing efficiently on bacteria as the only food
source, as is demonstrated by the high growth rate (0.14 h"1) and shorter doubling
times as compared to Cyclidium sp. and Stylonichia. Furthermore, Colpoda can
feed on picocyanobacteria {Synechococcus sp.), although the growth rate is 1.5-3
times lower than on bacteria (Table II).
The yield of Colpoda when fed on Synechococcus CN exceeded 104 Colpoda
cells ml"1, whereas when growing on the picoeukaryote, the yield was <103 cells
ml"1 (Figure 1). Thus, Colpoda grew poorly when fed on picoeukaryotes (Figure
1). The growth of Colpoda was inversely related to the growth of the prey
Synechococcus P (Figure 2), indicating the development of one population at the
expense of the other.
Three ciliates {Cyclidium, Colpoda and Stylonichia) were maintained on
bacteria TJO, and grazing was measured by FLB uptake (Figure 3). The rate of
FLB uptake was generally linear for the first 25 min. All grazing rates were calculated from the linear part of the curve. Calculated uptake values of bacteria per
ciliate per hour were 930, 35 and 1210 for Colpoda, Cyclidium and Stylonichia,
respectively.
When bacteria were the food source given to Colpoda, an increase in prey
concentration resulted in a decrease in clearance rates (405 to 32 nl cil"1 h"1). The
clearance rates on Synechococcus (P, CN) at prey concentrations of lOVlO* cells
ml"1 were in the range of 27-62 nl cil"1 h"1. Clearance values were much lower
Table IL Growth parameters of ciliates {Colpoda, Cyclidium, Stylonichia) on picoplankton
Picoplankton
Ciliates
M (h-')
dT(h)
Bacteria (T,o)
Colpoda
Cyclidium
Stylonichia
0.14
0.05
0.028
5
14
24.4
Synechococcus(P)
Colpoda
0.091
7.6
Synechococcus (CN)
Colpoda
0.047
1438
15
Grazing on atrtotrophic and heterotropfaic picoplankton
Fig. L Growth of the ciliate Colpoda steinii (104 ml"1) on autotrophic picoplankton. O—O, Synechococcus (CN); D—D, Synechococcus (P); A—A, picoeukaryote.
0
S
It
15
20
25
M
35
40
45
Fig. 2. Growth of Colpoda steinii (O) and Synechococcus P (•).
when the picoeukaryote was the food source (Table III). Concentrations of
picoplankton below 106 cells ml"1 resulted in lower uptake per ciliate, implying
dependence of grazing capacity on prey abundance.
Grazing rates of Colpoda at the same physiological stage depended on the type
and concentration of food given (Figure 4). At food concentrations of
1439
OMadasetal.
43
n
Styloniehia
30
<• Colpoda
15
^CydMram
IS
30
45
Time (min)
60
75
Fig. 3. Time course of uptake of FLBs by the ciliates: Stylonichia (D), Colpoda (•) and Cyclidium
(<>)•
10s—106 ml"1, higher and more persistent uptake was observed for Synechococcus
P than for Synechococcus CN. Uptake of picoeukaryotes per Colpoda was lower
than uptake rates for Synechococcus. At a cell concentration of 10* ml*1,
picoeukaryote uptake by Colpoda began only after 90 min, and no uptake was
observed until after 150 min when picoeukaryote concentration was 103 cells ml"1.
When labeled bacterium (Ti0) was the food source, concentrations of 10M.07
cells ml"1 resulted in the same range of bacteria uptake per Colpoda (930-1054)
(Figure 4, Table III). Stylonichia showed quite similar clearance rates (28-55 nl
ciH h~l), and population clearance (-0.0016 h"1) for the three types of picophytoplankton (Table IV). Compared to Colpoda (Table III), Cyclidium, which is
classified as a picoplankton feeder, showed lower clearance rates when fed on
Synechococcus P and bacteria (Table IV).
Generally, specific clearance (body volume cell"1 h"1) for the three ciliates
studied decreased when prey supply increased, and was not dependent on the
food source given. Specific clearance of Colpoda decreased from 1.5 X 106 to 9.7
x 103 when the prey (Synechococcus P) concentration increased from 103 to 107
cells ml"1. Grazing at concentrations of >107 cells ml"1 was impossible to follow
because of the high picocyanobacteria content within the Colpoda cells. The same
trend was found when Synechococcus CN served as the food source. Lowest
specific clearances were obtained (0.03-4.4 x 103) using picoeukaryotes. There
was no uptake of picoeukaryotes by Colpoda at prey concentrations below 104
cells ml"1 (Table V). Specific clearance for Cyclidium fed on Synechococcus P was
in the same range as for Colpoda. For Stylonichia, much lower values (<3 x 103)
for all the food sources used were recorded, implying poor feeding on picoplankton. From our results, it appears that, relating to body volumes, Colpoda could
manage successfully on bacteria as the sole food source (Table V).
1440
2
28.3
0.1 (n = 3)
l(n = 5)
0.1 (n = 2)
1 (n = 2)
0.1
l ( n = 3)
Bact
"± standard deviation.
Syn(P)
Syn(P)
Syn (CN)
Syn (CN)
Euk
Euk
pico x 106 ml-1
Picoplankton
2.3
37.7
3 ± 0.3*
4.67 ± 2.3
4.6 ± 0.57
3 ±1.7
2.4
4.06 ± 2.79
til X 103 ml-1
1054
930
5.25 ± 1.6
53.64 ± 4.8
6.15 ±1.91
26.85 ± 15.77
0.71
2.96 ± 2.06
Uptake
pico til"' h"1
Table ID. Colpoda consumption, grazing loss of picoplankton and clearance rates
405
31.6
52.8 ± 16.3
53.64 ± 4.8
61.5 ± 19.1
26.85 ± 15.77
7
2.96 ± 2.06
Clearance
nl cil-1 h"1
0.93
1.2
0.09 ± 0.08
0.246 ± 0.12
0.285 ± 0.12
0.094 ± 0.09
0.016
0.014 ± 0.015
Population
clearance h' 1
24
350
1.56 ±0.4
24.6 ±11.5
2.85 ± 1.2
9.4 ± 9.33
0.17
1.39 ± 1.5
Hourly grazing loss
pico x 104 ml*1 h-1
=
IS
time (min)
30
time (min)
30
45
45
60
60
Fig. 4. Grazing by Colpoda on different concentrations of picoplankton.
12 r
15
15
SO
time (min)
30
time (min)
45
100
ISO
Bact
Syn(P)
Syn(P)
Syn (CN)
Euk
Bact
Syn(P)
Stylonichia
Cyclidium
Picoplankton
Ciliate
17
0.18
1
1
1
7.28
0.19
pico x 106 ml"1
0.75
0.19
0.044
0.056
0.027
15.6
6.83
cil x 103 ml"1
1210
22.2
36.3
27.8
55.2
35
3
Uptake
pico cil-l h"1
67
124.7
36.3
28.2
55.2
4.3
15.5
Clearance
nl cil"1 h'1
Table IV. Stylonichia and Cyclidium consumption, grazing loss of picoplankton, and clearance rates
0.05
0.024
0.0016
0.0016
0.0015
0.067
0.106
Population
clearance rr1
9
4.3
1.6
1.6
1.5
5.4
0.2
Hourly grazing loss
pico x 104 ml"1 h*1
(XHadas et al.
Table V. Specific clearance by Colpoda fed on different concentrations of picoplankton
Picoplankton
cil x 10-1 ml"1
Bact
Bact
23
2
37.7
28.3
Syn(P)
Syn(P)
Syn(P)
Syn(P)
Syn(P)
3.4
3 ±0.3
4.6 ± 2.3
pico X 106 ml"1
0.001
0.1 (n = 3)
1 (n = 5)
3.8
10
4.75
100"
Syn(CN)
Syn(CN)
Syn(CN)
4.6 ± 0.57
3 ±1.7
Euk
Euk
Euk
Euk
Euk
2.4
2.9
2.4
1.7
4.06 ± 2.79
7
0.1 (« = 2)
1 (n = 2)
10
0.001"
0.01
0.1
1 (/• = 3)
22
Specific clearance
body vol cell"1 h"' x 103
135
11
1500
17.66 ± 5.7
17.98 ± 1.72
9.7
20.5 ± 6.36
8.7 ± 4.67
4.9
4.4
2.3
0.96 ± 0.67
0.03
T o o concentrated sample, impossible to count.
•Too dilute sample, no uptake until 150 min.
Discussion
Grazing by phagotrophic protozoa is considered a major factor controlling the
biomass and production of autotrophic and heterotrophic picoplankton in both
marine and freshwater systems (Iriberri et al, 1993; Simek et al, 1995). Several
authors have suggested that ciliates cannot survive in pelagic conditions on a diet
of bacteria only, but the organic carbon from picophytoplankton was not taken
into account (Fenchel, 1980; Rivier et al., 1985; Stockner, 1988; Sherr et al, 1991;
Weisse, 1993; Simek et al, 1996).
In our experiments, Colpoda steinii, which is denned as a bacterivore (Bick,
1972), grew rapidly with high growth efficiency on bacteria (TJO) alone, showing
growth rates of 0.14 h"1 and a doubling time of 5 h. When grown on picocyanobacteria (CN, P), growth rates ranged from 0.047 to 0.091 h"1 with doubling
times of 7.6-15 h. These doubling times were in the range found for large ciliates
by Fenchel (1987), and may vary among species according to resource availability
characteristic of their habitats. The two other ciliates studied, Stylonichia and
Cyclidium, had longer doubling times, suggesting that picoplankton are not
enough to supply their nutritional demands. We expected intensive feeding by
Cyclidium on bacteria since Cyclidium is known as a bacterivore (Fenchel, 1987;
Bick, 1972; Simek et al, 1995), but this was not found in our grazing experiments.
In another set of experiments using a flow cytometry technique, higher uptake of
FLB by Cyclidium was observed (unpublished data), which may show some problems with the FLB uptake in the former specific experiment. We could not
continue further grazing experiments because our Cyclidium culture died.
Growth rates recorded for another bacterivore ciliate, Strombidium sp.
1444
Grazing on autotrophic and heterotrophic picoplankton
(Oligotrichida), were 3-4 times higher when Strombidium was fed on bacteria
together with heterotrophic nanoflagellates, which might serve as an additional
food source for the ciliate (Ohman and Snyder, 1991). Furthermore, protozoa fed
on bacteria and Synechococcus are capable of regenerating nutrients (N, P),
which can be used by bacteria, resulting in an inverse oscillation pattern of the
two populations (Hadas et al, 1990). This oscillation pattern was observed in our
experiments on Synechococcus P and Colpoda (Figure 2). Stylonichia, known to
graze on algae and small protozoa (Bick, 1972), hardly grazed on picoplankton
at all, as expressed by the low specific clearance rates (0.5-2.2 x 103 tr 1 ), which
did not differ for the three food sources (bacteria, picocyanobacteria, picoeukaryotes), suggesting passive ingestion.
At concentrations of 2 X 106 bacteria ml"1 and 10s picocyanobacteria ml"1,
specific clearances of Colpoda were 1.3 x 105 h"1 and 2 x 10* h"1, respectively.
These concentrations of picoplankton are in the range encountered by Colpoda
under natural conditions in Lake Kinneret. Colpoda is generally abundant at the
thermocline in June, after the degradation of the Peridinium bloom, and the
following increase in heterotrophic bacterial numbers (Cavari and Hadas, 1979).
In autumn, a relatively dense population of ciliates, especially Coleps hirtus
(Madoni et al., 1990), is found at the chemocline zone in Lake Kinneret, probably
grazing on chemolithotrophic bacteria (O.Hadas, unpublished data). At this time,
epilimnic ciliates were full of picocyanobacteria, suggesting that picoplankton
were a significant component in the diet of the ciliate assemblage. Although the
high concentrations of ciliates applied in our experiments are rarely found in the
lake, the observed trends probably apply. Synechococcus CN and P enabled relatively high Colpoda yields, whereas picoeukaryotes could not sustain Colpoda
growth. This result may suggest a chemosensory evaluation of the prey and selective feeding behavior of the ciliates studied (Snyder, 1991). Ingestion rates of
bacteria by protozoa are probably influenced by different environmental and
biological factors such as temperature, initial prey concentration, the physiological state of prey and predator and bacterial production. In our comparative
grazing experiments, we used ciliates and picoplankton from the same batch
cultures. Colpoda clearance rates (nl cil"1 h"1) decreased with increasing concentrations of prey for all food sources tested (Table III). Grazing rates on picocyanobacteria were one order of magnitude lower than those on bacteria, as was
found by Simek et al. (1996). Relating to the body volume, only Colpoda (out of
the three ciliates tested) could manage with bacteria as the only food source.
In Lake Kinneret, bacterial abundance is in the range of lOMO7 cells ml"1,
varying with seasons. Growth rates found in our experiments are in good agreement with data obtained for ciliates in epilimnic waters of Lake Kinneret (Sherr
et al, 1991). Bacterial biovolume differs between the epilimnic water and the
hypolimnion where larger cells were observed (Schmaljohann et al., 1987). The
biovolume of bacteria in our experiments (0.4 um3) seem to be an average estimation of the values found in the lake. If in situ bacterioplankton are richer in
carbon than are their ciliate predators, ciliates will need to graze concomitantly
less bacterial biovolume to meet their food requirements. Cyclidium sp. isolated
from a reservoir in Bohemia preferred larger bacterioplankton cells and could
1445
(XHadas et al.
Table VL Carbon content of ciliates and carbon supplied to ciliates by consumed picoplankton1
Ciliate
C content1" Csupplied (pgCh- 1 )
(noC\
Bacteri:i Synechococcus P Synechococcus CN Picoeukaryote
Colpoda steinii
Cyclidium
Stytonichia
418
184
7970
81.8
3.1
106.5
32
0.6
4
16
ND
3.1
1.6
ND
ND
•Based on prey concentrations of 10*-107 ml"1.
b
Based on 1 urn* = 0.14 pg C.
grow in pelagic conditions exclusively on picoplankton of one doubling time
every 24-75 h (Simek et al., 1994,1995). It is assumed that protists are cropping
the production rather than the standing stocks of suspended bacteria because of
higher grazing pressure on larger cells of the assemblage (Gonzalez et al, 1993).
A central issue in food web studies is the efficiency with which ingested food is
converted into consumer biomass. A common measure of this quantity is gross
growth efficiency. In our calculations, we assumed a growth efficiency of 50% as
proposed by Fenchel (1987) and found for Lake Kinneret ciliates by Sherr et al.
(1991). Under this assumption, the carbon supplied by the consumed picoplankton (Table VI) would allow one doubling time in 10-26 h for Colpoda when
grazing on bacteria and Synechococcus P, respectively, and 52 h with Synechococcus CN. These results reinforce the conclusion that bacterial abundances in
Lake Kinneret ( l ^ - l O 7 bacteria ml"1) can sustain the carbon requirements of
Colpoda. If the same growth efficiencies are considered for Cyclidium and
Stylonichia grazing on bacteria, doubling times of 4-6 days would be required.
Shorter doubling times were recorded in our growth experiments (Table II), indicating higher growth efficiencies or higher carbon content of the bacteria than
were used in our calculations according to Lee and Fuhrman (1987). The carbon
supplied by the picophytoplankton was far below the requirements of these
ciliates and could not serve as a sole carbon source. In Lake Kinneret, ciliates
probably have other food sources, such as nanophytoplankton or different
picoplankton, than those used in this study.
Acknowledgements
The authors would like to thank Dr Paul Walline for reviewing the manuscript
and for the helpful comments. A part of this work is a partial fulfillment of
N.M.-R.'s PhD Thesis at Bar-Ilan University.
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Received on August 24,1997; accepted on March 24,1998
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