Journal of Plankton Research Vol.19 no.8 pp.979-993, 1997
Seasonal photosynthetic activity of autotrophic picoplankton in
Lake Kinneret, Israel
Nechama Z.Malinsky-Rushansky1-2, T.Berman 1 and Z.Dubinsky 2
'Israel Oceanographic and Limnological Research, The Yigal Allon Kinneret
Limnological Laboratory, PO Box 345, Tiberias, 14102 and 2Bar-Ilan University,
Department of Life Sciences, Ramat-Gan, Israel
Abstract. Autotrophic picoplankton populations in Lake Kinneret are composed of picocyanobacteria and picoeukaryotes. Overall, the rates of photosynthetic carbon fixed by autotrophic picoplankton during this study were low (0.01-1.5 mg C m~3 h"1). The highest chlorophyll photosynthetic activity
of the <3 (i.m cell-size fraction was found in spring, when picoeukaryotes predominated and in
addition small nanoplankton passed through the filters. The maximum cell-specific photosynthetic
rate of carbonfixationby picocyanobacteria and picoeukaryotes was 2.5 and 63 fg C cell"1 h"1, respectively. The highest specific carbon fixation rate of autotrophic picoplankton was 11 p.g C (ig~' Chi h~'.
The proportional contribution of autotrophic picoplankton to total photosynthesis usually increased
with depth. Picocyanobacteria collected from the dark, anaerobic hypolimnion were viable and
capable of active photosynthesis when incubated at water depths within the euphotic zone. Maximum
rates of photosynthesis (/"ma,) for picocyanobacteria ranged from 5.4 to 31.4 fg C cell"1 h~' with the
highest values in hypolimnetic samples exposed to irradiance. Photosynthetic efficiency (a) was -4fold higher in picocyanobacteria sampled from 40 m than in cells from near-surface waters. Light saturation (/fc) was lower in picocyanobacteria from 40 m, suggesting that these cells were acclimated to
lower light intensities. The relative contribution of autotrophic picoplankton to total phytoplankton
photosynthesis in Lake Kinneret was low, but occasionally, at seasons and depths where picocyanobacteria or picoeukaryotes were abundant, could account for most of photosynthetic activity.
Introduction
Since the advent of epifluorescence microscopy for the observation of micTobial
populations in the late 1970s, autotrophic picoplankton, or picophytoplankton
(<2 u,m), have been recognized as widespread marine and freshwater communities (Stockner, 1988). Autotrophic picoplankton populations include prokaryotic
cyanobacteria, frequently of the genus Synechococcus (Johnson and Sieburth,
1979; Waterbury et al, 1979), prochlorophytes (Chisholm et al, 1988), and small
eukaryotic cells (Johnson and Sieburth, 1982; Fahnenstiel et al., 1991b). Picophytoplankton are important contributors to total phytoplankton biomass and
primary production in oligotrophic environments (Johnson and Sieburth, 1979;
Li etal., 1983; Iturriaga and Mitchell, 1986), apparently decreasing in importance
with increasing nutrient levels (Craig, 1984; Stockner, 1988; Stockner and Shortreed, 1991). The contribution of oceanic autotrophic picoplankton to the total
standing stock of chlorophyll and to primary production may reach 80% (Platt et
al, 1983). Autotrophic picoplankton were responsible for 20-70% of total
primary productivity in a variety of freshwaters (Paerl and Mackenzie, 1977;
Fahnenstiel et al, 1986; Nagata et al, 1994; Chang and Petersen, 1995) with a
maximum of 95% reported by Craig (1984) in oligotrophic Little Round Lake.
Even in some extremely productive water bodies, 50% of the photosynthetic
activity was attributed to autotrophic picoplankton (e.g. Lake Balaton; Voros et
al., 1991). Much of the picoplankton production appears to be consumed within
© Oxford University Press
979
N.Z.Msilnsky-Rushansky, T.Berman and Z-Dubinsky
the photic zone by small heterotrophic protozoans (Sherr et al., 1986; Weisse,
1988) and phage-induced lysis has been suggested as an important factor limiting
the growth of autotrophic picoplankton (Klut and Stockner, 1990; Proctor and
Fuhrman, 1990).
As yet, there is little information about parameters, such as light saturation (7k),
photosynthetic efficiency at limiting light intensities (a), and photosynthesis at
saturating light intensities (Z1™,), which characterize autotrophic picoplankton
photosynthesis, especially in freshwater ecosystems.
Previous work on autotrophic picoplankton of Lake Kinneret is limited and has
focused on the abundance, biomass and growth rates (Malinsky-Rushansky and
Berman, 1991, 1995). The present study describes the photosynthetic activity of
the autotrophic picoplankton at different seasons and depths together with
photosynthetic parameters of the picocyanobacteria (7k, PmMX and a). The seasonal
and depth contribution of autotrophic picoplankton to total phytoplanktonic
primary production is outlined in relation to physical, chemical and biological
factors of the lake environment.
Lake site and methods
Lake Kinneret, in northern Israel, is a warm (13-30°C) monomictic lake, with a
surface area of 170 km2, and mean and maximum depths of 25 and 42 m, respectively. The main nutrient inputs from the catchment area occur during the winter
floods (November-April). With the onset of mixing, additional nitrogen (as
ammonia, NI-LJ and phosphorus (mostly soluble reactive phosphorus, SRP) from
the hypolimnion are transported into the photic zone. After seasonal stratification, which usually starts in April, the hypolimnion rapidly becomes anoxic,
with sulfide and NH, concentrations reaching 150-250 nM S and 35-90 \LM N,
respectively. Concentrations of bioavailable P and N in the epilimnion in
summer-fall are low, and are rapidly used by the biota (Pollingher et al., 1988).
SRP concentrations in the euphotic zone are usually <0.2 p,M.
Phytoplankton biomass in Lake Kinneret is dominated by the annual bloom
of the dinoflagellate Peridinium gatunense from mid-February until June
(Pollingher, 1981; Berman etal., 1992). Subsequently, during summer and fall, the
phytoplankton consists of nanoplanktonic chlorophytes, diatoms and a small proportion of cyanobacteria (up to 10% of total algal biomass), mainly represented
by Chroococcus minutus and Radiocystis geminata (Pollingher, 1991). At this
time, picocyanobacterial abundance is maximal, mostly Cyanodiction imperfectum (Hickel and Pollingher, 1988) and Synechococcus sp. (Malinsky-Rushansky
etal., 1995).
Chlorophyll a concentrations of autotrophic picoplankton were measured by
filtering lake water through 3 n-m Poretics polycarbonate membrane filters and
subsequently determining thefluorescenceof chlorophyll trapped on GF/F filters
and extracted by 90% acetone (Holm-Hansen et aL, 1965). Samples for microscopic examination of autotrophic picoplankton were immediately fixed with
formalin (final concentration 0.6%) and counted as described in MalinskyRushansky et al. (1995).
980
Seasonal photosynthetic activity of antotrophk picoplankton
Rates of photosynthetic carbon assimilation in Lake Kinneret were measured
during the year by a modified 14C uptake technique (Steemann-Nielsen, 1952;
Berman, 1973). Water samples were collected at a deep (40 m) central lake station
(A), representative of pelagic waters, from four depths in the euphotic zone (1,
5, 10 and 15 m) and at the metalimnion (-20 m) during thermal stratification.
After collection with a 5 1 Rhode-Aberg bottle, water was first filtered on board
through a 67 u,m pore size Nitex sieve to remove large grazers. Subsamples (100
ml) were then filtered by gravity in the dark through 3 p,m Poretics polycarbonate membrane filters into 120 ml clear glass bottles. When necessary, filters were
changed frequently to allow a slow, regular flow and to minimize retention of
autotrophic picoplankton on the filters. Radioactive carbon (NaH14CO,; Amersham) was added to a final concentration of 0.1 u,Ci ml"1. The samples, together
with dark controls, were incubated in situ at their original depth for 3 h (from
-09:00 to -12:00 h), and brought to the laboratory in the dark within 30 min.
Replicate samples (50 ml) were filtered on 0.2 (im cellulose filters (Sartorius), at
low (<50 mmHg) vacuum pressure. The filters were fumed with HC1 in order to
remove unassimilated inorganic radioactive carbon, and placed in scintillation
cocktail liquid (70% xylene and 30% Lumax). Radioactivity was counted with a
Kontron MR 300 liquid scintillation counter with a counting efficiency of 90%.
To differentiate between photoassimilation and dark carbon assimilation, the
radioactivity on filters from dark bottles was subtracted from light bottles. Controls for non-biological adsorption of 14C to particles were prepared with samples
poisoned by adding Lugol's iodine prior to radioactive carbon. Total inorganic
carbon (TIC) was determined using alkalinity and pH values, as described in
Standard Methods (American Public Health Association, 1989). Rates of carbon
assimilation are given per hour, and not per day, because of the possible variations in activity during daylight hours (Happey-Wood, 1994).
In order to determine the contribution of picocyanobacterial chlorophyll and
photosynthetic activity to the <3 um fraction, water samples (May 1992) were
passed through filters of 3 and 1 u.m pore size. Previous experiments had shown
that picoeukaryotes did not pass through filters of 1 u.m pore size; therefore, we
assume that the <1 u,m fraction was mainly picocyanobacteria.
In November 1992, when picocyanobacterial numbers were relatively high
(>104 cells ml"1) in the dark anaerobic hypolimnion (Malinsky-Rushansky et al,
1995), we measured the potential for photosynthetic carbon assimilation by picocyanobacteria taken from 40 m and incubated at different depths in the euphotic
zone (Figure 3). Pre-filtered water from these same depths was also incubated in
situ. Picoeukaryotes were not found at that period in the lake, so the results were
attributed to picocyanobacteria.
To calculate photosynthetic parameters of picocyanobacteria, we generated
photosynthesis versus irradiance (P versus I) curves with lake water samples,
taken in November 1992. Replicate samples from 0,5 and 40 m were spiked with
[14C]NaHCO3 (final concentration of 0.1 u,Ci ml"1) and incubated in glass scintillation vials, at six light intensities (0,35,60,110,170 and 900 u.E nr 2 s"1). PmMX was
the rate of carbon assimilation at saturating light intensity; a, an index for photosynthetic efficiency at limiting light intensities, was calculated as the linear region
981
N.ZJUalmsky-RiJshansky, T.Berman and Z-Dobinsky
of the Pll relationship; 7k, the photosynthetic acclimation parameter, was the
intensity at which the initial rising part of the curve intersected with Pnax. Dark
carbon fixation was taken as the _y-intercept at zero light intensity. P,^, a, 7k and
the dark fixation are given as fg C cell"1 h"1, fg C cell"1 h"1 ^E" 1 m2 s, n-E m~2 s'1
and fg C cell"1 h"1, respectively.
Results
In the present work, the term autotrophic picoplankton will be used for prokaryotic and eukaryotic organisms which carry out oxygenic photosynthesis and pass
through 3 jim filters. Throughout the year and at all depths, autotrophic picoplankton (<3 urn) consisted of picocyanobacteria and/or picoeukaryotes.
Picocyanobacteria were abundant at fall, while picoeukaryotes were found in
winter and spring (Table I). Chlorophyll a concentrations of the <3 ^m fraction
ranged from -0.1 to 1.0 jjug H. In June 1991, chlorophyll a (<3 u.m) was low (0.1
H-g I"1). By September 1991, chlorophyll a (<3 u.m) had risen and was evenly distributed in the upper 15 m. In January and March 1992, the abundance of picocyanobacterial and picoeukaryotic cells was minimal. In April 1992, autotrophic
picoplankton chlorophyll was high, due to the occurrence of picoeukaryotes.
Autotrophic picoplankton chlorophyll accounted for 0.7-13.3% of total chlorophyll. When only picocyanobacteria were present (September and October 1991),
cell-specific chlorophyll increased with depth (Table I).
Details of the photosynthetic activity associated with the picoplankton fraction,
measured on seven dates, from June 1991 through May 1992, are shown in Table
II. Activity was high (1.53 mg C Ir 1 m~3) at 5 m in October 1991, when picocyanobacteria were most abundant (Malinsky-Rushansky et aL, 1995). At this
time, the contribution of autotrophic picoplankton to total photosynthesis
increased with depth, reaching 100% at 10-15 m. Relatively high autotrophic
picoplankton photosynthesis was found in June 1991, when picoeukaryotes predominated, accompanied by low numbers of picocyanobacteria. In winter 1992,
low photosynthetic activity and contribution to total photosynthesis (0.8-3% at
1-10 m and 14% at 15 m) was found. Some of the photosynthetic activity recorded
in April 1992, in near-surface waters (1 and 5 m), was also due to small nanoplanktonic algae, such as Chrysochromulina parva, Rhodomonas minuta and Cyclotella
polymorpha (Meyer and Hakansson, 1996; U.PoUingher personal communication), which passed through the 3 jim filter, as observed in microscopic examination. Despite the decrease in autotrophic picoplankton cell numbers, the
photosynthetic activity associated with the <3 jim fraction was high at the thermocline (15-20 m) in June through September. The contribution of autotrophic
picoplankton to total photosynthesis (as a percentage) usually increased with
depth (Table II).
Photosynthetic activity, chlorophyll and cell numbers, associated with
autotrophic picoplankton, at 5 m depth are shown in Figure 1. Chlorophyll and
photosynthesis (<3 (im) were high from August 1991 until November 1991, when
only picocyanobacteria were present in the lake, and maximal in April-May 1992,
when picoeukaryotes dominated and picocyanobacterial cell numbers were low.
982
Seasonal pbotosyntfaetk activity of autotrophic pkoplankton
Table L Chlorophyll (p.g H ) and cell numbers (ml"1) associated with the <3 um fraction
Cyano1 (mh1)
Eukb (mi-1) fg Chi cell-1
Depth (m)
Date
Chi
% of total Chi
1
5
10
15
20
4 June 91
0.1
0.1
0.1
0.1
0.1
1.6
0.7
0.7
1.0
ND
415
1100
480
109
87
295
415
611
240
65
125
49
78
298
711
1
5
10
15
20
19 Sept. 91
0.9
1.0
0.9
1.0
0.3
9.0
9.1
8.6
8.7
ND
645 000
390 000
300 000
300 000
74 000
NF
NF
NF
NF
NF
1
2
3
3
4
1
5
10
15
20
8 Oct. 91
0.5
0.4
0.4
0.5
0.2
5.8
4.9
4.9
6.9
ND
629 000
621000
568 000
454 000
141000
NF
NF
NF
NF
NF
1
1
1
1
1
1
5
10
15
20
28 Oct. 91
0.7
0.6
0.5
0.7
ND
8.2
6.9
6.5
8.1
ND
360 000
298 000
254 000
295 000
430 000
NF
NF
NF
NF
NF
2
2
2
2
ND
1
5
10
15
20
8 Jan. 92
0.2
0.2
0.2
0.2
0.2
6.4
8.9
9.9
13.3
ND
4441
6153
6742
6032
1900
100
63
42
42
NF
43
28
26
36
95
1
5
10
15
20
2 March 92
0.2
0.2
0.2
0.2
0.2
6.1
6.9
9.1
9.2
ND
1100
920
58
130
NF
44
NF
166
210
NF
909
NF
1
5
10
15
20
28 April 92
0.6
0.6
0.4
0.1
ND
2.2
1.8
1.6
1.2
ND
130
175
160
22
ND
4985
3600
2019
3068
ND
NF
220
NF
NF
NF
22
22
ND
ND, no data; NF, not found.
"Picocyanobacteria.
b
Picoeukaryotes.
Photosynthesis (<3 u.m) at 5 m was minimal from December 1991 until March
1992, when picocyanobacterial and picoeukaryote numbers were low.
In May 1992, picocyanobacterial photosynthesis was low at most depths, contributing minimally (2.7%) in near-surface waters, but at 5 m, it accounted for
almost all of the autotrophic picoplankton photosynthesis (Figure 2). Picocyanobacterial chlorophyll accounted for 3.5% (at 1 m) to 16.1% (at 10 m) of
autotrophic picoplankton chlorophyll. In near-surface waters (0-2 m), most of the
983
N.ZJVlaHnsky-Rushiuisk^T.Bcniuiii and Z.Dublnjky
Table IL Autotrophic picoplankton: photosynthetic carbon assimilation and contribution to total algal
photosynthesis
m g C i n-3 h-1 % of total
photosynthesis
Depth (m)
mg C nr 3 h"1 % of total
photosynthesis
1
5
10
15
20
4 June 91
1.04
0.75
0.08
0.30
0.74
4.1
3.2
2.1
1.2
37.1
28 Oct. 91
0.83
0.76
0.05
0.10
ND
2.6
4.8
4.4
43.5
ND
1
5
10
15
20
19 Sept. 91 0.12
0.23
0.06
NF
0.88
0.8
1.7
7.3
NF
ND
2 March 92
0.36
0.06
0.01
0.04
NF
3.0
1.0
0.8
14.2
NF
1
5
10
15
20
8 Oct. 91
8.3
22.9
98.8
100.0
NF
28 April 92
22.52"
1.10
0.23
0.49
ND
46.1"
21.1
28.6
82.2
ND
0.92
1.53
0.51
0.29
NF
ND, no data; NF, not found.
•In this sample, many small nanoplankton which had passed through the 3 urn filter were observed.
photosynthetic activity found in the fraction >1 and <3 (xm was probably due to
the presence of small nanoplankton.
Specific carbon fixation rates of autotrophic picoplankton during this study
varied from 0.05 to 11 \ig C jig"1 CM h-1 (Table III). The photosynthetic rates
were normalized to chlorophyll, and not cell numbers, because we could not differentiate between picocyanobacteria and picoeukaryotes when both were
present. When we found only picocyanobacteria (e.g. in September and October
1991), the specific assimilation numbers ranged from 0.07 to 1.9 u.g C u-gr1 Chi
per cell. When we observed only picoeukaryotes (28 April 1992 at 5 m), the
specific assimilation number was 1.7 jig C n-g"1 Chi per cell.
The cell-specific photosynthetic activity (as fg C cell"1 h"1) of picocyanobacteria
taken from 40 m, and incubated in situ at 1 and 5 m, was ~8- and 4-fold higher,
respectively, than that in water from the original sample depths (Figure 3). The
activity of these samples at 1 m was lower than at 5 m, probably because of photoinhibition. When an additional experiment was carried out in November 1992,
the effect of photoinhibition was more pronounced (Table IV). At 0 and 5 m,
assimilation numbers for picocyanobacteria from 40 m were -15- and 5-fold
higher, respectively, than those for samples taken and incubated at the original
depths. Assimilation numbers were lower at 0 m, suggesting that both the surface
picocyanobacteria, and those taken from 40 m and incubated at 0 m, were photoinhibited.
Photosynthetic parameters derived from P versus / curves for picocyanobacteria from 0,5 and 40 m, in November 1992, are given in Table V. Photosynthetic
efficiency (a) was higher in picocyanobacteria from 40 m compared to those from
0 and 5 m. /*„,„ ranged from 6.4 to 31.4 fg C cell"1 h"1, with the highest values in
samples from 40 m. Light saturation was lower for samples from 40 m compared
984
Seasonal photosynthetic activity of autotrophic picoplankton
J
J
A
8
O
N
D
J
F
M
A
M
1S00
1EHM
1100
I
J
J
A
S
O
N
D
J
F
M
A
M
month
Fig. L (A) Lake Kinneret autotrophic picoplankton photosynthetic activity ( • , mg C nr 3 Ir 1 ) and
chlorophyll (x, p,g H) at 5 m depth. (B) Picocyanobacteria (•, log cells mh1) and picoeukaryotes ( • ,
cells mF).
to 0 and 5 m. Dark carbon fixation, corrected for poisoned samples, was -8-fold
higher in samples from 40 m and may have been partially due to bacterial
chemosynthetic activity.
Discussion
Picocyanobacteria in Lake Kinneret were dominant during the summer and fall
in the epilimnion. At this time, available P and N are low, and picocyanobacteria
985
Rnshansky, XBerman and Z-Dobinsky
chlorophyll (%)
0
6
12
18
£
Q.
3
0
20 40
60
80 100
photosynthesis (%)
Fig. 2. Contribution (%) of picocyanobacteria to autotrophic picoplankton photosynthetic activity
and chlorophyll a in Lake Kinneret (May 1992). +, % picocyanobacteria] chlorophyll; x, % picocyanobacterial photosynthesis.
may have a competitive growth advantage due to their higher surface to volume
ratio and subsequent higher efficiency in nutrient uptake (Wehr, 1990). Furthermore, Badger et al. (1994) and Kaplan et al. (1990) showed that cyanobacteria
possess a CO2-concentrating mechanism, which elevates CO2 around the active
site of the carbon-fixing enzyme ribulose 1,5 bisphosphate carboxylase/oxygenase
(Rubisco), enhancing photosynthetic performance when CO2 is limited. In Lake
Kinneret after the dinoflagellate bloom, aqueous CO2 is limiting (Berman-Frank
et aL, 1994) and this situation could give an additional advantage to picocyanobacteria. Abundant picocyanobacterial cells (>104 cells ml-1) were found in
the dark anaerobic hypolimnion which were viable and able to photosynthesize
actively when exposed to different levels of irradiance. Picoeukaryotes were
mostly present in winter and spring, when there are higher nutrient levels in the
Table HL Specific photosynthetic carbon assimilation (ug C ugr1 Chi h"1) of autotrophic picoplankton
in Lake Kinneret
Depth (m)
June 91
Sept. 91
Oct. 91
Jan. 92
March 92
April 92
May 92
1
5
10
15
20
1-11
2-11
0.1-1
0.1-3
03-7
0.1
0.2
0.1
NF
3.4
1.2-1.9
1.2-3.5
0.1-1.2
0.1-0.6
NF
NF
03
NF
NF
1.9
1.9
03
0.1
02
NF
ND
1.7
0.6
3.7
ND
ND
0.7
2
0.6
ND
NF, not found; ND, no data.
986
Seasonal photosynthetk activity of antotrophic pkoplankton
fgC coir1 h 1
20
0.01
0.1
Fig. 3. Lake Kinneret: autotrophic picoplankton photosynthetic activity (fg C cell"1 h~r) at 1,5,10 and
15 m.+, in situ samples; x, samples relocated from 40 m; • , downwelling photosynthetically available
irradiance ((iE s"1 nr 2 ).
lake. Sondergaard (1990) noted that picoeukaryotes dominated from February
until August in Danish eutrophic and humic lakes, with a shift to picocyanobacterial dominance when conditions became more oligotrophic.
The concentrations of chlorophyll associated with autotrophic picoplankton in
Lake Kinneret were in the range of results observed in other freshwater studies
(Table VI). Relatively high chlorophyll values were found in September-October
1991, when there were large numbers of picocyanobacteria (>105 cells ml"1), and
in spring 1992, when picoeukaryotes dominated. Cell-specific chlorophyll (as fg
Table IV. Photosynthetic parameters of picocyanobacteria in Lake Kinneret
Depth (m)
0
5
In situ sample
Relocated 40 m sample
b
Ps"
Chl
1.8-1.9
12.1-12^
9.0-10.0
6.8-6.9
A.N.<
Ps
Chi
A.N.
0.19-0.2
1.78-1.83
6.7-8.0
27.4-28.9
3.1-3.9
3.1-3.9
1.9-2.2
7.6-8.0
•Photosynthesis as fg C cell-1 h"1.
•"Chlorophyll a as fg celh1.
c
Assimilation numbers as jig C ngr1 Chi h~'.
Results are given as the range of duplicate samples.
987
N.Z.Matinsky-Rushansky, T.Bennan and ZJhibinsky
Table V. P versus / parameters for picocyanobacteria in Lake Kinneret
Depth (m)
Initial slope*
Light saturation15
1
0
5
40
0.049
0.046
0512
110
95
60
5.4
6.4
31.4
c
P
max
Dark fixation"1
4.6
1.0
39.7
•fg C cell"1 h"1 ulE-" m2 s.
nEms.
c
fg C celh1 h"1 (after subtraction of dark uptake).
d
fg C cell"1 h"1 (calculated from y-intercept of the P versus / curve).
cell"1) was >100-fold higher in spring (from 100 to 5000) when picoeukaryotes
dominated, compared to other times in the year when picocyanobacterial cells
were very abundant. These values were typical for picoeukaryotes and Synechococcus sp. isolated from the lake and grown in cultures. Furthermore, in May
1992, when we differentiated between picocyanobacteria (<1 u.m) and picoeukaryotes (>1 and <3 u,m), the cellular chlorophyll content of the latter was also
100-fold higher. Chlorophyll per cell can be overestimated because the chlorophyll of the <3 u.m fraction filtered through GF/F filters could be derived not only
from autotrophic picoplankton, but also from small nanoplankton and photosynthetic bacteria, while the numbers of autotrophic picoplankton cells were
obtained with direct counting by epifluorescence. In Danish Lakes, Sondergaard
(1990) also noted that sometimes cells ~4 u,m passed through 2 u,m filters, and
picophytoplankton cell numbers were overestimated.
When the lake was stratified, we found an increase in chlorophyll a per cell with
depth. Sampling was carried out at 09:00 h in the morning after calm conditions
and probably no significant wind occurred earlier, suggesting a stable water
column and photoacclimation by cells with depth through the euphotic zone. In
winter, when the whole water column was mixed, we observed no increase in cellspecific chlorophyll levels with depth.
The rates of photosynthetic carbon fixation by autotrophic picoplankton in the
lake from June 1991 until April 1992 were low and ranged from 0.06 to 1.5 mg C
nr 3 h"1 when only picocyanobacteria were present (September-October 1991), and
from 0.4 to 1.1 mg C m~3 h"1 when picoeukaryotes dominated (April 1992 at 5 m,
May 1992 at 15 m). These rates in Lake Kinneret were comparable to those
reported in other studies (Table VI). The maximum rate of cell-specific primary
production for picocyanobacteria and picoeukaryotes in Lake Kinneret was 2.5 and
6.3 fg C cell"1 h"1, respectively, similar to rates found in Lakes Superior, Huron and
Michigan (Fahnenstiel etaL, 1986,1991a), but much lower than values reported for
extremely productive Lake Balaton (100 fg C celh1 h"1; Voros et aL, 1991).
The very high photosynthetic activities found in April and May 1992 in the
near-surface waters were due in part to small flagellate algae, abundant at this
time, such as C.parva and R.minuta, which passed through the 3 u-m filters and
which are able to optimize light absorption by active vertical swimming. At 5 m
and below, photosynthetic activity decreased, probably due to light shading by
the dinoflagellates.
988
Seasonal photosynthetic activity of aaf otrophlc picopUnkton
Table VL Autotrophic picoplankton photosynthesis and chlorophyll from different studies
Reference and site
Chang and Petersen, 1995
LakeTahoe
Craig, 1984
Little Round Lake
Fahnenstielera£,1986
Lake Superior
Fahnenstiel and Carrick, 1992
Lakes Huron and
Michigan
Happey-Wood, 1994
Llyn Padam
Iturriaga and Mitchell, 1986
Open ocean
Nagatarta/,,1994
Lake Baikal
Pick and Agbetti, 1991
Sharpe's Bay, Ontario
Ray etaL, 1989
Chesapeake Bay
Sondergaard, 1990
Danish Lakes
Stockner and Shortreed, 1991
British Columbia
Yukon lakes
This study
Lake Kinneret
Trophy
Season
Max phot
<3 um
% of total
photosynthesis
Chl(MgH)
oligo
May-Sept.
2.28
34-69
0.12-0.47
oligo
Mid-autumn
_
>95
-
oligo
May-Oct.
0.31*
50
-
oligo
oligo
March-Nov.
March-Nov.
-
>40
-
meso
Aug-Sept.
1.6"
41
4.17-5.5
oligo
-
2.6-3.8b
45-SO
0.12-0.5
oligo
Late July
29.2b
19-80
-
meso
May-Sept.
3.8"
33-47
0.5-0.13
oligo
Summer
5"
9-13
oligo
meso
eu
Feb-Aug.
Feb-Aug.
Feb-Aug.
-
-
1.3-7.4
0.3-15
0-65.7
oligo
April-Nov.
-
29-53
0.34-1.08
1.53*
>95
0.1-1
(10-15 m in Oct.)
meso-eu Jan-Dec.
23
oligo, oligotrophic; meso, mesotrophic; eu, eutrophic.
•mgCm-'h-1.
•
m"3 day 1 .
In the metalimnion, some of the photosynthetic activity associated with the <3
u,m fraction may have been due to photosynthetic bacteria, e.g. Thiocapsa
roseopersicina, Rhodomonas palustris and Chlorobium phaeobacteroides (Butow
and Bergstein-Ben Dan, 1992) rather than to picocyanobacteria or picoeukaryotes.
The assimilation numbers for autotrophic picoplankton observed in Lake Kinneret were within the range of values reported for marine and freshwater studies
by Stockner (1988), by Iturriaga and Mitchell (1986) in the open ocean, and by
Ray et al. (1989) in Chesapeake Bay (0.3-14.5, 2-2.7, 2.1 and 2.5 (ig C n.g"1 Chi
h"1, respectively). The maximum assimilation number was 11 jig C u-g"1 Chi h"1
and was similar to those reported by Chang and Petersen (1995) for Lake Tahoe.
In May 1992, in Lake Kinneret near-surface waters, picocyanobacterial photosynthesis (<1 u.m cell si2e fraction) accounted for only 1-2%, while the <3 p,m
fraction accounted for -40% of total photosynthesis. During the annual Peridinium bloom, the photosynthetic contribution of the autotrophic picoplankton
was low at depths where Peridinium dominated, but in deeper waters where the
989
N.7-MnHmiky.Ritdiainfcy, T.Bennan and Z-Dobinsky
larger algae were affected by shading from intense surface patches of Peridinium
and lessened specific light absorption, the importance of the small algae
increased. At 5 m, almost all autotrophic picoplankton photosynthetic activity
was due to picocyanobacteria, which were growing at their optimal light level (28
2 1
JJLE rrr s" ). Autotrophic picoplankton photosynthetic activity at 10-15 m was due
mostly to picoeukaryotes. In Lake Superior, the contribution of the <3 u.m fraction to total carbon fixed (-50%) was quite similar to our results, but the contribution of the <1 u.m fraction (16-24%) was higher (Fahnenstiel et al, 1986). In
Lakes Huron and Michigan, autotrophic picoplankton photosynthesis in the <3
and <1 u.m fractions accounted for 21-65% and 6-43% of primary production,
respectively, with similar results for both surface and deep-water samples
(Fahnenstiel et al, 1991a). Iturriaga and Mitchell (1986) found that picocyanobacteria contributed from 45 to 80% of total photosynthesis in the open ocean.
In Chesapeake Bay, photosynthesis by the <3 u,m fraction was 5-17% and was
inversely related to light intensity (Ray etal., 1989).
In Lake Kinneret, in fall, when only picocyanobacteria were present, photosynthetic rates at saturating light level (P^,) and light saturation values (/k) were
in the range of those observed in Lakes Huron, Michigan and Superior (Fahnenstiel etal, 1986,1991a; Fahnenstiel and Carrick, 1992). In our study, /k values were
60 and -110 JJLE m~2 s"1 for samples from 40 and 0-5 m, respectively, suggesting
that picocyanobacteria from 40 m were acclimated to lower light intensities. Low
/k values were also reported by Chang and Petersen (1995) for picophytoplankton in Lake Tahoe, but in the open ocean and the Gulf of Maine, Iturriaga and
Mitchell (1986) and Glover et al (1985) found /k above 150 n-E nr 2 s"1.
Picocyanobacterial cells from 40 m may have been nutrient replete in the nutrient-rich hypolimnion, in contrast to picocyanobacteria in the relatively nutrientdepleted epilimnion. In previous work, we suggested that the major source for
picocyanobacteria in the hypolimnion in fall was sedimentation and perhaps
advection by currents from the littoral (Malinsky-Rushansky et al, 1995). It is
probable that these cells, when reaching the photic zone after mixing of the water
column, become an inoculum for the picocyanobacteria which develop when
favorable conditions, such as higher water temperatures, occur in summer-fall.
In the central Baltic Sea, Detmer et al. (1993) noted that cellular primary production of the deep water samples was enhanced by the rise in temperature and
by higher phosphate and ammonia concentrations. In Lake Biwa, at least 105 cells
cm"'3 of phototrophic phytoplankton in the bottom sediments were in a viable
state when grown at 50 u.E m"2s~! (Eguchi et al, 1996).
The relative contribution of autotrophic picoplankton to total phytoplankton
photosynthesis in Lake Kinneret was low, but occasionally, at depths where picocyanobacteria or picoeukaryotes were abundant, could account for almost all
photosynthetic activity. The proportion of photosynthetic contribution by autotrophic picoplankton is greater in oligotrophic rather than in meso-eutrophic
waters (Craig, 1984; Fahnenstiel et al, 1986; Stockner, 1988), but even in extremely productive water bodies, picoplankton may contribute markedly (50%)
to total photosynthetic activity in summer, if not restricted by factors such as N
limitation or zooplankton grazing (Voros et al, 1991). In other studies, the
990
Seasonal photosynthetic actirity of antotrophic pkoplankton
autotrophic picoplankton contribution to total photosynthesis ranged from 29 to
95% in freshwater ecosystems (Table VI). Most of these results are derived from
relatively short-term observations, generally in the period from spring to fall,
when autotrophic picoplankton abundance is maximal. Only a few studies differentiate between the separate contribution of picoeukaryotes and picocyanobacteria. In temperate Sharpe's Bay, Pick and Agbetti (1991) reported a
maximum photosynthetic contribution of autotrophic picoplankton of 33% in
late summer when picocyanobacteria dominated, and 47% in spring when
picoeukaryotes dominated.
Autotrophic picoplankton appear to be particularly well adapted to low light
levels. Kirk (1983) reported that the specific absorption of light per milligram of
chlorophyll a increases as the cell or colony diameter decreases, because of lower
'package effect'. In our study, high cell numbers and photosynthetic activity
found at 5 m (in September-October 1991 and January 1992) corresponded to
light intensities that were relatively low (<40 JJLE nr 2 s"1) and found to be optimal
for autotrophic picoplankton in cultures (N.Z.Malinsky-Rushansky, unpublished
results).
The autotrophic picoplankton contribution to total primary production in the
euphotic zone of Lake Kinneret tended to increase with depth. Similar trends
have been observed in many freshwater and marine ecosystems (Li et al, 1983;
Platt et al, 1983; Craig, 1984; Glover et al, 1985; Voros et al, 1991) reflecting, in
part, the greater efficiency of picocyanobacterial photopigments in absorbing
blue-green light, especially in oceanic waters (Li et al, 1983; Glover et al, 1985;
Wood, 1985) and of picoeukaryotes to utilize blue light. Phycoerythrin-rich
cyanobacteria have developed chromatic adaptation to the quality and intensity
of light available at the oceanic depths where they normally occur (Wood, 1985).
However, in Lake Kinneret, we did not find phycoerythrin-containing picocyanobacteria and the increased contribution of autotrophic picoplankton to total
photosynthesis with depth depended on the decreased contribution of other
phytoplankton at those depths.
Acknowledgements
The authors wish to thank Dr Y.Z.Yacobi for providing data on phytoplankton
photosynthesis, Prof U.Pollingher for useful discussions, and M.Hatab and
V.Harel, the crew of the Hermona. This work is in partial fulfilment of N.Z.Malinsky-Rushansky's requirements for a PhD thesis at Bar-Dan University and was
supported by Grant 1932-1-93 from the Ministry of Science and the Arts,
Jerusalem, Israel, by a grant (No. 87-00006) from the US-Israel Binational
Science Foundation, Jerusalem, Israel and by the Israel Water Commissioner. A
contribution of Israel Oceanographic & Limnological Research.
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Received on August 3, 1996; accepted on March 26, 1997
993