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Influence of abiotic and biotic factors on
microcystin content in Microcystis
aeruginosa cells in a eutrophic temperate
reservoir
KATARZYNA IZYDORCZYK1*, TOMASZ JURCZAK2, ADRIANNA WOJTAL-FRANKIEWICZ2, ALEKSANDRA SKOWRON1,
JOANNA MANKIEWICZ-BOCZEK1 AND MAłGORZATA TARCZYŃSKA2
1
INTERNATIONAL CENTRE FOR ECOLOGY, POLISH ACADEMY OF SCIENCES,
UNIVERSITY OF LODZ,
3
TYLNA,
90-364
2
LODZ, POLAND AND DEPARTMENT OF APPLIED ECOLOGY,
12/16 BANACHA, 90-237 LODZ, POLAND
*CORRESPONDING AUTHOR: [email protected]
Received October 18, 2007; accepted in principle December 17, 2007; accepted for publication January 10, 2008; published online
January 27, 2008
Corresponding editor: Roger Harris
The Sulejow Reservoir (Poland) was sampled on a weekly basis between May and September in
2003 and 2004 to examine changes in weight-specific microcystin content of Microcystis
aeruginosa and to examine which abiotic or biotic factors may be the key factors governing microcystin content. The variables examined in this study included: temperature; total and dissolved
inorganic phosphorus and nitrogen; and Daphnia biomass. Comparing summertime from both
years, despite the similar levels of cyanobacterial biomass, a significant difference between microcystin concentrations was observed which resulted from a difference in microcystin content.
Differences in weight-specific microcystin content were discussed in relation to different Daphnia
biomass (r ¼ 0.34, n ¼ 40, P , 0.05). It is possible that exposure to Daphnia and/or
chemical signals released by predators may have resulted in increased microcystin content of M. aeruginosa. Nevertheless, the influence of weight-specific microcystin content on microcystin concentrations (r ¼ 0.56, n ¼ 40, P , 0.05) was less than that of cyanobacterial biomass (r ¼
0.82, n ¼ 40, P , 0.05), which was strongly correlated with temperature and phosphorus
ability. This study indicated that not only abiotic factors, but also the presence of herbivorous zooplankton, may determine microcystin content of M. aeruginosa.
I N T RO D U C T I O N
Microcystis aeruginosa blooms are widespread in eutrophic
lakes and reservoirs of the world. Microcystins, toxins
produced by Microcystis and other cyanobacterial genera,
can be harmful to aquatic organisms and humans
(Chorus and Bartram, 1999; Falconer, 2005). Some of
these toxins are known tumour promoters and have
been associated with high rates of primary liver cancer
(Fujiki et al., 1996). The concentration of microcystin in
water depends on cyanobacterial biomass and the
specific toxicity of the cyanobacteria present.
The influence of abiotic factors on microcystin production by cyanobacteria has been extensively studied.
Investigations of Microcystis cultures have shown that
microcystin production by cyanobacteria depends on
such parameters as light intensity, temperature and
availability of nutrients (for a review see Rapala, 1998).
Nevertheless, the effects of nitrogen and phosphorus on
microcystin production are highly variable and sometimes contradictory (Watanabe and Oishi, 1985; Kotak
et al., 1995; Oh et al., 2000; Kameyama et al., 2002;
Vezie et al., 2002). However, changes in microcystin
doi:10.1093/plankt/fbn006, available online at www.plankt.oxfordjournals.org
# The Author 2008. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
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content of cyanobacteria are still not fully understood,
especially if natural ecosystems are considered (Kotak
et al., 2000; Graham et al., 2004; Giani et al., 2005).
Interestingly, Jang et al. (Jang et al., 2003) suggested
that cyanobacterial toxin production responds to zooplankton feeding activity, which conforms to the
hypothesis that microcystin acts as a protective compound against grazing by zooplankton (DeMott, 1999).
The aim of our study was to evaluate changes in
weight-specific microcystin content of M. aeruginosa in
the Sulejow Reservoir over two years to determine
which abiotic or biotic factors may be key to governing
microcystin content. The variables examined in this
study include: temperature, total and dissolved inorganic phosphorus and nitrogen, and Daphnia biomass.
METHOD
The Sulejow Reservoir is a shallow, eutrophic reservoir
situated in central Poland in the middle course of the
Pilica River. There are two main tributaries supplying
water to the Sulejow Reservoir: The Pilica River and
the Luciaza River. At full capacity the reservoir has an
area of 22 km2, mean depth of 3.3 m and volume of
75106 m3. Mean water retention time is 30 days. The
shoreline length is 54 km, of which 34.5 km is
forested (Wagner and Zalewski, 2000). The Sulejow
Reservoir has been extensively studied (Zalewski et al.,
1990, 2000; Zalewski, 2006). The dominant species of
bloom-forming cyanobacteria is M. aeruginosa, which
produces microcystin-LR, -YR and -RR (Tarczynska
et al., 2001; Jurczak et al., 2004, 2005;
Mankiewicz-Boczek et al., 2006).
Integrated water samples were taken using a 5-litre
sampler from each meter of the entire water column.
Integrated water samples were collected weekly from
May to September in 2003 and 2004 at a pelagic
sampling station in the lower part of the reservoir. The
samples were taken at 11 a.m. During the sampling,
water temperature in a vertical profile, as well as wind
direction and speed, were measured.
Total phosphorus (TP) and phosphate phosphorus
(P-PO4) were measured by the ascorbic acid method
(Golterman et al., 1978). Total nitrogen was analysed
using the persulfate digestion method (method no.
10071; HACH, 1997). Nitrate nitrogen (N-NO3) was
determined using the cadmium reduction method
(method no. 8039; HACH, 1997) and ammonium
(N-NH4) was determined using the phenate method
(Golterman et al., 1978).
Water samples for phytoplankton assessment were
preserved in Lugol’s solution and sedimented in the
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laboratory. Additionally, Microcystis colonies were disintegrated (Cronberg, 1982). Phytoplankton was counted
using a Fusch– Rosenthal counting cell. At least 400
cells or filaments were counted to reduce the error to
,10% (P ¼ 0.05). The phytoplankton biomass (fresh
weight) was determined based on a volumetric analysis
of cells using geometric approximation. Biomass
computed in volume units was transposed to fresh
biomass assuming the density of phytoplankton as 1
(Komarkowa et al., 1995).
Microcystin concentrations in water [mg L21] were
analysed in two forms—dissolved in water and cellbound in suspended matter. For dissolved microcystin,
1 litre of filtered water sample was concentrated by the
Baker (Netherlands) solid phase extraction system and
eluted from C18 cartridges by 90% aqueous methanol
with 0.1% trifluoroacetic acid. Methanol was evaporated and sample was redissolved in 1 ml of 75%
aqueous methanol before HPLC analysis (Jurczak
et al., 2005). However, the extracellular concentration
of microcystin in the reservoir water was negligible
and was disregarded. For the HPLC analysis of intracellular microcystin, 1 litre water samples containing
cyanobacterial material were filtered immediately after
sampling through Whatman GF/C filters. The
preparation of cyanobacterial material and determination of microcystin by HPLC – DAD were performed
according to previous description (Meriluoto and
Codd, 2005).
In order to examine weight-specific microcystin
content [mg mg21 fresh weight], the ratio between concentration of intracellular microcystin (represented
microcystin concentrations within the cyanobacterial
cells per litre of lake water [mg L21]) and biomass of
cyanobacteria per litre of lake water [mg L21] was
calculated.
A specific volume of water (generally 30 L ¼ 5 litre
per each meter of the entire water column) was filtered
through a 50 mm net to concentrate zooplankton,
which were then preserved in Lugol’s solution.
Zooplankton were counted over the whole area of a
1 mL counting cell (0 – 200 ind. mL21). Biomass for
particular zooplankton genera (wet weight) was estimated based on species-specific length/weight
regressions (Bottrell et al., 1976; Horn, 1991).
All variables in the statistical analyses were first analysed for homogeneity of variance and normality.
Log-transformation of data did not prove to be sufficient for the use of parametric tests. Therefore, relationships between cyanobacterial biomass, microcystin
concentration and content and environmental variables
were developed using Spearman rank order correlations. Differences between summertime data (from
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INFLUENCE OF ABIOTIC AND BIOTIC FACTORS ON MICROCYSTIN CONTENT
late July through September—the period when cyanobacterial blooms occurred in both years) were tested
using Wilcoxon match pairs test with a significance level
of P , 0.05.
R E S U LT S
Dynamics of cyanobacterial biomass,
microcystin concentration and
content
The cyanobacterial blooms in the Sulejow Reservoir
were dominated (98%) by M. aeruginosa. M. viridis,
M. wesenbergii, Aphanizomenon flos-aquae and Pseudanabaena
sp. also occurred, however, their biomass remained at a
very low level. In 2003, two peaks of cyanobacterial
biomass were observed (Fig. 1a). The first peak was
observed in June, which was untypical for a eutrophic
temperate reservoir, and the second was a typical
peak in August. Cyanobacterial biomass in June
reached maximum values of 34 mg L21, whereas in
August it ranged between 14 and 29 mg L21. In 2004,
cyanobacterial biomass increased by the end of
July, and the summertime maximum of 33 mg L21
occurred in the middle of August. Cyanobacterial
biomass ranged between 16 and 30 mg L21 in August
and early September and declined to below 5 mg L21
by late September. Comparing summertime in both
years, the average cyanobacterial biomass was similar
(Table I).
Despite the similar levels of cyanobacterial biomass,
microcystin concentrations were significantly lower in
summer 2003 than in 2004 (Table I). In 2003, two
peaks of microcystin concentration were observed.
High microcystin concentration was coincident with
increasing cyanobacterial biomass, corresponding
with peaks in cyanobacterial biomass (Fig. 1b). A
maximum of 2.86 mg L21 was observed in June,
whereas in August microcystin concentration ranged
between 1.13 and 1.90 mg L21. In 2004, microcystin
was detected from late July, and in August and
September the concentration ranged between 2.01
and 5.83 mg L21.
During summer 2003, the average weight-specific
microcystin content was significantly lower than in 2004
(Table I). However, in both years, the maximum values
were similar: 0.57 and 0.58 mg mg21, respectively
(Fig. 1c).
The study demonstrated a positive correlation
between microcystin concentration in water and cyanobacterial biomass (r ¼ 0.82, n ¼ 40, P , 0.05), as well
as between microcystin concentration in water and
weight-specific microcystin content (r ¼ 0.56, n ¼ 40,
P , 0.05) (Table II.).
Physical and chemical conditions
These two years were characterized by different thermal
conditions in the reservoir. In 2003, water temperature in
late spring exceeded 208C and reached a maximum
value of 24.48C on June 18. High temperatures in the
range 22–238C occurred from the middle of July
through August. Water temperature decreased in
September and fell to 17–198C. The year 2004 was
characterized by low temperatures in May and June that
did not exceeded 198C. Water temperature increased to
218C by the end of July and remained at that level until
the middle of September, when it declined below 158C.
Nevertheless, there was no significant difference between
average temperatures during summers (Table I).
TP concentrations ranged from 4.8 to 14.2 mM from
May through mid-July in 2003, whereas during the
same period in 2004 they ranged from 1.6 to 3.2 mM.
The concentrations of P-PO4 corresponded with TP
concentrations. Higher P-PO4 concentrations were
detected from May through mid-July 2003 (1.3–
2.6 mM) than in 2004 (0.6– 1.6 mM). There were no
significant differences in range or mean total and
P-PO4 concentrations between late July through
September in 2003 and 2004 (Table I).
Total nitrogen concentrations ranged from 121 to
185 mM from May through mid-July 2003, whereas in
2004, they ranged from 21 to 128 mM. From late July
through September, TN concentrations were higher in
2003 than in 2004, but no significant differences were
found (P , 0.01) (Table I). Higher N-NO3 concentrations were detected from May through mid-July in
2003 (50– 160 mM) than in 2004 (0.2– 1.3 mM). There
was no significant difference in N-NO3 concentration
during the summers (Table I). N-NH4 concentrations
were similar in both years, but were higher in summer
2003 than in 2004 (P , 0.05) (Table I).
Dynamics of zooplankton biomass
Analysis of zooplankton biomass showed that cladocerans, Daphnia cucullata and D. longispina, were the dominant species in the herbivorous zooplankton community
in the Sulejow Reservoir (56 and 75%, respectively). In
2003, Daphnia biomass ranged between 0.35 and
8.75 mg L21, excluding two times when it reached
16.6 mg L21 (May 21) and 13.78 mg L21 (July 31)
(Fig. 1d). In 2004, Daphnia biomass fluctuated from 3.4
to 30.3 mg L21. During summer 2003, Daphnia biomass
was significantly lower than in 2004 (Table I).
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Fig. 1. Seasonal dynamics in (A) cyanobacterial biomass, (B) microcystin concentration, (C) weight-specific microcystin content and (D) Daphnia
biomass in the Sulejow Reservoir during 2003 (closed triangles) and 2004 (open circles).
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Table I: Differences between summertime in both years (results of Wilcoxon matched pairs test; bold
indicates significance at P , 0.01)
Mean + SD for
summer 2003
21
Cyanobacterial biomass [mg L ]
Microcystin concentration [mg L21]
Weight-specific microcystin content
[mg mg21 fresh weight]
Temperature [ºC]
TP [mM]
P-PO4 [mM]
TN [mM]
N-NH4 [mM]
N-NO3 [mM]
Daphnia biomass [mg L21]
Small cladocerans biomass [mg L21]
Zooplankton biomass [mg L21]
Mean + SD for
summer 2004
T
n
P-level
12.1 + 9.0
0.88 + 0.68
0.08 + 0.04
15.3 + 10.0
3.34 + 1.53
0.28 + 0.15
27.00
0.00
0.00
11
11
11
0.594
0.003
0.003
20.4 + 2.4
6.3 + 3.2
2. 7 + 0.3
122.7 + 35.1
5.2 + 3.3
61.2 + 38.2
4.45 + 4.02
5.90 + 8.85
10.34 + 12.09
19. 8 + 2.6
5.7 + 3.6
3.1 + 1.7
82.5 + 49.8
3.3 + 2.7
35.7 + 25.9
13.74 + 5.12
4.67 + 2.4
18.41 + 5.30
25.00
31.00
54.54
13.00
9.00
9.00
0.00
21.00
11.00
11
11
11
11
11
11
11
11
11
0.477
0.858
1.000
0.075
0.033
0.109
0.003
0.286
0.051
Table II: Spearman rank order correlation
between cyanobacterial biomass, microcystin
concentration and weight-specific microcystin
content, and some abiotic and biotic variables
based on whole vegetation season data
( ¼ 40, bold indicate significance at
P , 0.05)
Cyanobacterial
biomass
Cyanobacterial
biomass
Microcystin
concentration
Weight-specific
microcystin content
Temperature
TP
P-PO4
TN
N-NH4
N-NO3
Daphnia biomass
Small cladocerans
biomass
Zooplankton biomass
Weight-specific
Microcystin
microcystin
concentration content
–
0.82
0.10
0.82
–
0.56
0.10
0.56
–
0.51
0.49
0.59
0.13
20.03
20.10
20.09
0.13
0.36
0.40
0.60
20.06
20.23
20.20
0.14
0.31
20.03
0.09
0.26
20.27
20.16
20.22
0.34
0.22
0.03
0.21
0.31
Daphnia was accompanied by small cladocerans:
Bosmina sp., Alona sp., Chydorus sp., which had similar
biomass in both years (Table I).
DISCUSSION
Seasonal (within year) variations of weight-specific
microcystin content were observed in both years, but
significant differences were observed comparing these
two years. Comparing summertime in both years,
despite the similar level of cyanobacterial biomass, a
significant difference between microcystin concentrations was observed, which resulted from a difference
in microcystin production. Significant differences in
weight-specific microcystin content during summertime
corresponded with significant differences in Daphnia
biomass between years. Additionally, during the hot
spring of 2003, the low point of zooplankton population
was coincident with increasing cyanobacterial biomass,
but microcystin content was low. In contrast, during the
following spring, the high biomass of large bodied zooplankton, D. cucullata and D. longispina were coincident
with low cyanobacterial biomass and high microcystin
content. We found a statistically significant correlation
between weight-specific microcystin content and Daphnia
biomass (r ¼ 0.34, n ¼ 40, P ¼ 0.033, Table II). It is
possible that exposure to Daphnia and/or chemical
signals released by predators at higher population
density may have resulted in the observed increased
weight-specific microcystin content of M. aeruginosa,
though influence of chemical signals cannot be directly
demonstrated from these results.
Our results seem to support the hypothesis of Jang
et al. (Jang et al., 2003). Jang et al. showed experimentally
that contact with zooplankton or chemicals released by
zooplankton increased toxin production in cyanobacteria. All four strains of M. aeruginosa increased
microcystin production in the presence of zooplankton
and/or filtrates from zooplankton cultures. Selander
et al. (Selander et al., 2006) showed that the marine dinoflagellate Alexandrium minutum cells were able to detect
and respond to waterborne signals from a natural
enemy by inducing an increased production of paralytic
shellfish toxins. This supported the “info-chemical” or
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chemical cue hypothesis, which states that chemical
signals released by predators can induce defences in
aquatic prey (Bronmark and Hansson, 2000). This
chemical cue may be a metabolite resulting from the
feeding activity of the zooplankton or a substance
released from crustacean tissue (Hansson, 1996).
Properties of chemical cues are not constant; for
instance, Selander et al. (Selander et al., 2006) showed
differences in response between algae exposed to cues
from the starving and feeding copepods, which may
have resulted from different release rates of the cues.
There are only a few other investigations of grazerinduced responses in phytoplankton, e.g. colony formation in Scenedesmus (Hessen and van Donk, 1993;
Verschoor et al., 2004) or life history changes in dinoflagellates (Rengefors et al., 1998). Verschoor et al.
(Verschoor et al., 2004), in an experiment that used
water after removal of zooplankton, observed colony
formation in Scenedesmaceae in response to infochemicals produced by herbivorous zooplankton.
Rengefors et al. (Rengefors et al., 1998) showed that a
chemical cue, indicating the presence of zooplankton,
was enough to restrain or delay germination of both
Ceratium and Peridinium cysts. Consequently, it may determine succession and composition of phytoplankton
communities.
Induced response may also be an important factor in
formation of harmful algal blooms as suggested by
Selander et al. (Selander et al., 2006). They showed that
the increased toxin content of the algal cells correlated
to an increased resistance of dinoflagellates to grazing
by the copepod Acartia tonsa. A study of the
cyanobacterial-zooplankton interaction, which focused
on cladoceran tolerance to toxic Microcystis, reported
that filtrators coexisting with cyanobacteria are more
resistant to their toxins than organisms that were never
exposed to them (Hietala et al., 1995; DeMott, 1999).
Investigations by Guo and Xie (Guo and Xie, 2006)
showed increased resistance of cladocerans to toxic food
after exposure to Microcystis. This suggests the possibility
of development of gradual adaptive evolution in grazing
zooplankton as a response to toxins.
The majority of the studies performed on cyanobacterial toxin production have been done under laboratory conditions. Our field observations were performed
under natural, more complex conditions where the
effects of zooplankton or chemical cue from zooplankton occurred together with the effects of abiotic factors
such as nutrient availability.
Responses of microcystin production to phosphorus
were studied in culture experiments. Codd and Poon
(Codd and Poon, 1988), Oh et al. (Oh et al., 2000) and
Kameyama et al. (Kameyama et al., 2002) found that
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decreasing concentration of phosphorus increased
microcystin production by Microcystis. Contrary to results
obtained from laboratory experiments, we observed a
positive trend between weight-specific microcystin
content and increasing P-PO4 (Table II), which is consistent with a study by Giani et al. (Giani et al., 2005).
They reported that when cells are not nutrient-limited,
the microcystin content of producing cells does not vary
significantly with changes in external nutrient supply.
They analysed samples from 22 lakes in southern
Quebec with a wide trophic range and suggested that
control of microcystin production by phosphorus is of
negligible importance among lakes, but that increases in
phosphorus act by enhancing the relative contribution
of toxigenic cyanobacteria to total phytoplankton
biomass. Our results seemed to support this hypothesis.
The strong positive correlation between TP and P-PO4
and both cyanobacterial biomass and microcystin concentration was observed (Table II), which is consistent
with other field studies (Kotak et al., 1995, 2000; Jacoby
et al., 2000; Graham et al., 2004).
Nitrogen availability is also an important factor
affecting microcystin production, as we might expect,
for peptide synthesis. Some authors, based on culture
experiments, showed that the microcystin content of
M. aeruginosa was positively correlated with nitrogen
content in growth medium (Watanabe and Oishi, 1985;
Lee et al., 2000). Nevertheless, Kotak et al. (Kotak et al.,
2000), based on preliminary laboratory study, suggested
that microcystin production is not a response to nitrogen limitation stress. We observed a negative trend
between total and dissolved form of nitrogen and both
microcystin content and concentration (Table II). This
might be interpreted as intensive consumption for toxin
production.
Investigations of Microcystis cultures have also shown
that microcystin production of cyanobacteria also
depends on temperature. During our investigation,
water temperature in the reservoir ranged between 18
and 258C, which included the optimum temperature
range for toxin production (Codd and Poon, 1988;
Rapala, 1998). However, low microcystin content was
observed when water temperature was .228C,
especially during spring 2003. Higher microcystin
content was detected when the temperature decreased
,188C during September 2004. Although we did not
find a correlation between temperature and weightspecific microcystin content, positive correlations
between temperature and both cyanobacterial biomass
and microcystin concentration were observed (Table II).
In particular, high water temperature during spring
2003 may have been the cause of early cyanobacterial
bloom occurrence, which was untypical for a eutrophic,
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temperate reservoir. This had an impact on microcystin
concentration in the reservoir by increasing the volume
and size of the population producing microcystin.
The current study contributes to understanding the
key factors governing microcystin production in the
eutrophic Sulejow Reservoir. Our investigation indicated
that the abiotic factors of temperature and phosphorus
availability, through the stimulation of cyanobacterial
growth, were not the only factors related to increased
microcystin concentration in the reservoir. The concentration of microcystin also depended on the specific toxicity of the cyanobacteria present. Significant differences
in weight-specific microcystin content between years
corresponded with different Daphnia biomass. It is possible that exposure to zooplankton and/or chemical
signals released by predators may have resulted in
increased weight-specific microcystin content of M. aeruginosa. Nevertheless, it is very hard to infer causalities
from field observations, and further tests are necessary
to confirm the relationship between microcystin content
and grazing by zooplankton. Knowledge of the interaction between cyanobacterial toxicity and the presence
of zooplankton is essential to understanding the possibility and consequence of top-down control for effective
reservoir management.
Chorus, I. and Bartram, J. (1999) Toxic Cyanobacteria in Water. A Guide to
their Public Health Consequences, Monitoring and Management. E&FN Spon
on behalf of the World Health Organization., London, pp. 416 (eds).
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Cronberg, G. (1982) Changes in the phytoplankton of Lake Trummen
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Falconer, I. R. (2005) Cyanobacterial Toxins of Drinking Water Supplies:
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Giani, A., Bird, D. F., Prairie, Y. T. et al. (2005) Empirical study of cyanobacterial toxicity along a trophic gradient of lakes. Can. J. Fish.
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AC K N OW L E D G E M E N T S
The authors are grateful to Professor Ian R. Falconer,
Professor Maciej Zalewski and anonymous referees for
comments that substantially improved the manuscript.
We thank Sebastian Ratajski for their substantial help in
sampling.
FUNDING
This research was supported by the European
Commission ( project EC-EVK1-2001-00 182 acronym
TOXIC) and the Polish Committee of Scientific
Research ( project 2 PO4F 044 27).
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