Features of Structural Changes in the Plankton Community of an Alpine Lake with Increasing Fish Density in Summer and Autumn

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ISSN 1062-3590, Biology Bulletin, 2021, Vol. 48, No. 8, pp. 1272–1283. © Pleiades Publishing, Inc., 2021.
Russian Text © The Author(s), 2021, published in Zoologicheskii Zhurnal, 2021, Vol. 100, No. 2, pp. 147–158.
Features of Structural Changes in the Plankton Community
of an Alpine Lake with Increasing Fish Density
in Summer and Autumn
A. V. Krylova, *, A. O. Hayrapetyanb, D. B. Kosolapova, E. G. Sakharovaa, N. G. Kosolapovaa,
R. Z. Sabitovaa, M. I. Malina, I. P. Malinaa, Yu. V. Gerasimova, A. A. Hovsepyanb,
L. R. Gambaryanb, A. S. Mamyanb, S. E. Bolotova, A. I. Tsvetkova, S. A. Hakobyanb,
S. A. Poddubnya, and B. K. Gabrielyanb
a Papanin Institute for the Biology of Inland Waters, Russian Academy of Sciences,
Borok, Nekouzskii raion, Yaroslavl oblast, 152742 Russia
b Institute of Hydroecology and Ichthyology, Scientific Center of Zoology and Hydroecology,
National Academy of Sciences of Armenia, Yerevan, 0014 Republic of Armenia
*e-mail: krylov@ibiw.ru
Received July 9, 2019; revised November 10, 2019; accepted January 30, 2020
Abstract—It is found that a large species of the order Cladocera, Daphnia (Ctenodaphnia) magna Straus, has
disappeared from the zooplankton composition in the alpine Lake Sevan, Armenia, with an increase in the
density of whitefish, Coregonus lavaretus L. This led to an increase in the quantitative characteristics of het-
erotrophic nanoflagellates, resulting in a decrease in the number and biomass of bacterioplankton. At the
same time, a number of seasonal features of plankton transformation were observed. In particular, the num-
ber and biomass of planktonic invertebrates, including representatives of Cladocera, D. longispina
O.F. Müller, and Diaphanosoma lacustris Kořínek increased in July. The main reason for this was the change
in the distribution of whitefish caused by an increase in their abundance, depletion of food supply due to the
disappearance of D. magna, and a high water temperature. This contributed to the formation of the maximum
fish density at greater depths than usual, where the trophic and temperature conditions were optimally com-
bined. The reduction of a significant effect of fish on zooplankton can be associated with an increase in the
trophic status of the lake under which grazing is compensated by a higher fecundity of invertebrates. An
increase in the trophic status of the lake is indicated by an increase in the phytoplankton biomass, which is
determined by the increasing amount of phosphorus regenerated by Cladocera against the background of a
high water temperature. This not only compensated for grazing of algae and cyanobacteria, but also contrib-
uted to an increase in their biomass. In October, the pressure of fish on invertebrates in the water column
increased due to an increase in their density and the patterns of their vertical distribution due to oxygen defi-
ciency in the near-bottom layers. Under these conditions, the number of species and the proportion of Roti-
fera in the total abundance and biomass of zooplankton increased, while the total abundance and biomass of
zooplankton decreased due to the filter-feeding crustaceans D. lacustris and D. longispina. However, the
decrease in their abundance did not lead to changes in the biomass and structure of phytoplankton, which is
associated with the decrease in the input of phosphorus excreted by Cladocera. Thus, the response of inver-
tebrates and the groups of planktonic organisms they control to an increased density of the fish population
depends on the vertical distribution of planktophages determined by the water temperature, oxygen concen-
tration, and the quantitative characteristics of food objects.
Keywords: alpine Lake Sevan (Armenia), quantitative characteristics, structure, zooplankton, phytoplank-
ton, bacterioplankton, heterotrophic nanof lagellates, fish density, water temperature, oxygen concentration
DOI: 10.1134/S1062359021080161
INTRODUCTION
Lake Sevan is an alpine (~1900 m above sea level)
water body with the greatest area (~1262 km2) in the
Caucasus located between 40°18′38.16′′ N,
45°20′57.12′′ E. In 1978, Sevan National Park was
founded under the Ramsar Convection.
Since 2002, the ecological state of the lake has been
determined by the scheduled water level rise and fluc-
tuation in the density of the fish population mainly
formed by whitefish (Coregonus lavaretus L.) and
Prussian carp (Carassius auratus gibelio (Bloch))
(Ozero Sevan …, 2016). These factors contributed to
transformation of the zooplankton, which plays a cru-

BIOLOGY BULLETIN Vol. 48 No. 8 2021
FEATURES OF STRUCTURAL CHANGES IN THE PLANKTON COMMUNITY 1273
cial role in the formation of the structure of the plank-
tonic community in the lake. Of particular importance
are Cladocera, which are represented in Lake Sevan by
the native species Daphnia longispina O.F. Müller and
two alien species, Diaphаnosoma lacustris Kořínek
(since 2005) and Daphnia (Ctenodaphnia) magna
Straus (since 2011) (Krylov et al., 2016, 2016a, 2018).
The maximum quantitative characteristics of cladoc-
erans were reached due to D. magna during the period
of a significant reduction in the whitefish abundance
in 2011 and 2012 (Ozero Sevan …, 2016). However, a
gradual decrease in the fish density started in 2013,
which promotes study of the changes in invertebrates
and other components of the lake plankton as an
urgent task. The results of the study of plankton in
Lake Sevan at different fish densities against the back-
ground of changes in a number of abiotic environmen-
tal factors may become the basis for predicting the
state of biological communities of water bodies in con-
ditions of fluctuations in the quantitative characteris-
tics of the highest trophic level.
The aim of this study is to describe changes in the spe-
cies composition, quantitative parameters, and structure
of planktonic organisms in Lake Sevan at different fish
densities in the summer and autumn seasons.
MATERIALS AND METHODS
The primary material was collected at 15–20 sta-
tions in the pelagic zone (>15 m) in Bolshoi (BS) and
Malyi Sevan (MS) in July and October 2013 and 2018.
Zooplankton samples were collected by a vertical tow
from the bottom to the surface using a Juday net and a
4-L Molchanov bathometer every 1–5 m. The sam-
ples were fixed in 4% formaldehyde; laboratory pro-
cessing was performed according to the common
method (Metodika…, 1975); the biomass was calcu-
lated using the size of organisms (Balushkina and Vin-
berg, 1979). Excretion of mineral phosphorus by Cla-
docera was estimated according to the equations of the
dependence of the animal body weight on water tem-
perature (Zhukova, 1989). Integrated samples of phy-
toplankton, bacterioplankton, and heterotrophic
nanoflagellates were taken with a Molchanov bathom-
eter from the surface to the bottom every 1–5 m. The
preservation and laboratory analysis of phytoplankton
samples were carried out according to the standard
procedure (Metodika…, 1975). To obtain samples of
bacterioplankton and heterotrophic nanoflagellates,
water samples were fixed with 40% formaldehyde
immediately after sampling to a final concentration of
2% and stored in the dark at 4°С. The number and size
of microorganisms were estimated using epifluores-
cence microscopy (Olympus BX51 (Japan)). Bacteria
were stained with DAPI fluorochrome (Porter and
Feig, 1980); nanoflagellates were stained with prim-
ulin (Caron, 1983). The wet biomass of microorgan-
isms was calculated by multiplying their abundance by
the average cell volume. The spatial distribution of the
fish population in the lake was determined by the
hydroacoustic method (Simmonds and MacLennan,
2005; Parker-Stetter et al., 2009) using a scientific
SIMRAD EK80 echosounder with a dual-frequency
ES38-18/200-18C transducer (split beam at 38 kHz,
single beam at 200 kHz, beam angle at 18° for both fre-
quencies). The survey was carried out along pre-
planned transects aboard the RV Gidrolog at a speed of
3 m/s; the transducer was submerged 1 m below the
water surface. The echo counting method was used to
analyze the fish distribution in the depth range from
2.5 m to the bottom. Fish were caught with multimesh
gillnets that consisted of six panels of monofilament
nylon that were each 6 m long and 10 m high. The pan-
els were of different mesh sizes and were sewn together
in the following order: 35, 20, 40, 25, 45, 30 mm. Fish-
ing was carried out in close proximity to the dump of
depths (distance from the shore, 1.5 km, the depth of
the lake at the fishing site, 28 m). The nets were cast at
two horizons: in the depth range of 0–10 and 10–20 m.
In the whitefish sampled, the digestive tracts were
extracted and fixed in 96% ethanol. The composition
of the content of the digestive tracts was determined
under a binocular microscope. The water transpar-
ency was measured with a Secchi disk. The water tem-
perature and oxygen concentration at depths from 0 to
30 m every 1–5 m were measured with a YSI ProPlus
meter, and the water temperature in the layer deeper
than 30 m was measured with a thermometer.
In the statistical analysis we used the Kolmog-
orov–Smirnov test to check for the normality of the
distribution; the significance of differences was esti-
mated by one-way analysis of variance (p < 0.05,
ANOVA); the least significance difference (LSD) test
was used to compare the means of multiple groups; the
strength of the relationship between variables was
measured using the Pearson correlation coefficient
(p< 0.05).
RESULTS
July. In 2018, the water transparency decreased and
its temperature was higher than in 2013; in MC by 1.1–
2.0°С to the depth of 30 m, in BS, by 1.2–3.3°С (Table 1,
Figs. 1а, 1b). Measurements of the dissolved oxygen
concentration conducted only in BS showed that its
concentration in the entire water column was higher
than 4 mg/L (Fig. 1c).
In 2018, the phytoplankton biomass, abundance,
and biomass of heterotrophic nanoflagellates
increased and the bacterioplankton abundance and
biomass decreased compared to 2013 (Table 1). In
2013, the phytoplankton biomass was basically formed
by Chlorophyta (58.4% in MS and 51.5% in BS); in
2018, by Cyanophyta (52.9 and 50.8%); and the pro-
portion of Bacillariophyta decreased (from 15.3 to
0.5% and from 12.4 to 0.7%). Solitary cells <2 μm pre-
vailed in bacterioplankton in terms of abundance: in
2013, 97.7% in MS, 97.6% in BS; in 2018, 98.3 and

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BIOLOGY BULLETIN Vol. 48 No. 8 2021
KRYLOV et al.
Table 1. Average (m ± SD) water temperature and transparency, abundance (N), and biomass (В) of phyto- (PhP), bacterioplankton (BP), and heterotrophic nano-
flagellates (HNF) in Malyi (MS) and Bolshoi (BS) Sevan in July and October 2013 and 2018
Here and in Tables 2 and 3: * indicates significant differences according to LSD-test (p < 0.05).
Parameter
July October
MS BS MS BS
2013а2018b2013с2018d2013e2018f2013g2018h
Water temperature, °С 19.4 ± 0.2*b21.4 ± 0.2*d19.5 ± 0.1*d22.1 ± 0.3 13.6 ± 0.1*f,g 15.7 ± 0.6 14.7 ± 0.2*h16.5 ± 0.2
Water transparency, m 11.8 ± 0.7*b2.1 ± 0.8 10.5 ± 0.6*d2.3 ± 0.6 11.2 ± 0.1*f8.6 ± 0.3 8.6 ± 0.4 8.0 ± 0.3
PhP В, g/m30.49 ± 0.12*b2.38 ± 0.59 0.33 ± 0.15*d2.23 ± 0.26 0.87 ± 0.1 0.92 ± 0.2 1.05 ± 0.3 1.12 ± 0.3
BP N, 103 cells/mL 8999.8 ± 1563.8*b4669.1 ± 1564.8 11118.7 ± 1608.7*d4138.7 ± 501.8 10203.1 ± 2545.7*f2901.9 ± 412.1 13326.4 ± 678.0*h3584.6 ± 247.3
В, mg/m3546.7 ± 55.6*b235.6 ± 29.59 505.8 ± 65.8*d258.0 ± 39.4 797.7 ± 120.4*f284.1 ± 28.6 1168.6 ± 313.6*h277.7 ± 22.2
HNF N, cells/mL 88.6 ± 29.5*b724.6 ± 170.4 64.7 ± 30.4*d692.6 ± 152.6 193.5 ± 112.9*f567.6 ± 40.3 271.9 ± 55.7*h585.7 ± 93.5
B, mg/m36.9 ± 2.2*b42.3 ± 14.6 5.2 ± 2.5*d32.7 ± 10.9 8.8 ± 5.1*f,g 27.7 ± 5.9 25.6 ± 5.1*h29.0 ± 6.6

BIOLOGY BULLETIN Vol. 48 No. 8 2021
FEATURES OF STRUCTURAL CHANGES IN THE PLANKTON COMMUNITY 1275
Fig. 1. Vertical distribution of temperature in (а) Malyi and (b) Bolshoi Sevan and (c) dissolved oxygen: I, July 2013; II, July 2018;
III, October 2013; IV, October 2018.
60
50
40
30
20
10
0 25155 2010
m°C
III
III IV 30
25
20
15
5
10
0 25155 2010
°C
30
25
20
15
5
10
01062 84 mg/
L
(a) (b) (c)
96.9%, respectively. The biomass was mainly formed
by cells of <2 μm; however, in 2013, their proportion
was 92.9% in MS and 93.0% in BS and in 2018, it
decreased to 82.6 and 75.5%, respectively, due to an
increasing proportion of cells of >2 μm.
In 2013 and 2018, the abundance of Rotifera was
higher in zooplankton in BS; in 2013, the abundance
of Cladocera was lower (Table 2). In 2013, the abun-
dance was mainly formed by Copepoda, while in 2018,
the pronounced predominance of a particular group of
invertebrates was not found. In 2013, Hexarthra mira
(Hudson) and nauplii and copepodites of Calanoida
and Cyclopoida, Cyclops strenuus (Fischer) and Daph-
nia longispina, dominated in term of abundance; in
2018, Euchlanis dilatata Ehrenberg, Daphnia
longispina, Diaphanosoma lacustris, and nauplii of
Calanoida were dominant; in MS there were also
copepodites of Calanoida and in BS, Keratella
quadrata (Müller) and Filinia terminalis (Plate). In
2018, the Shannon index calculated using abundance
increased and the total abundance of zooplankton
increased due to Rotifera and Cladocera.
Cladocera largely contributed to the zooplankton
biomass (Table 2). In 2013, Daphnia magna and
D. longispina dominated in terms of biomass; in 2018,
D. longispina prevailed only in MS and there were also
Diaphanosoma lacustris, Cyclops strenuous, and Acan-
thodiaptomus denticornis (Wierzejski); in BS, there was
Cyclops abyssorum. In 2018, the biomass of Rotifera
and Copepoda and the proportion of Cladocera in the
total biomass of zooplankton increased compared to
the data obtained in 2013 (Table 2). In addition, in
2018, Daphnia magna disappeared from the commu-
nity but the abundance and biomass of D. longispina
and Diaphanosoma lacustris and the amount of phos-
phorus excreted by them increased (Table 3).
The density of the fish distribution differed between
the two parts of the lake: the maximum value was
recorded in BS, 40.6 (2013) and 428.0 (2018) ind./mln
m3, whereas in MS, it was 7.7 and 84.2 ind./mln m3,
respectively. In 2013, the majority of the fish popula-
tion (56.1% in MS and 64.0% in BS) was concentrated
in a 10- to 15-m water layer (Figs. 2a, 2c). At the same
time, the maximum fish density (35.7%) in MS was
recorded at a depth of 14–15 m (water temperature
18.3°С), while in BS, this occurred at a depth of 10–11 m
(25.6, water temperature 18.7°С) (Figs. 1а; 2а, 2c). In
2018, the fish population was concentrated in deep
water layers: in MS, from 15 to 21 m (85.3%), and in
BS, at depths within 6–21 m (88.6%) (Figs. 2а, 2c).
The maximum fish density in MS was recorded at the
horizon of 18–19 m (32.8%, water temperature
17. 7 °С), and in BS, at the depth of 18–19 m (19.3%,
water temperature 7.6–9.0°С) (Figs. 1b; 2а, 2c). The
fish concentration at these depths in 2018 is confirmed
by the analysis of their horizontal distribution: the
largest accumulations both in MS and BS were found
at the depth dump in the area of 20 m (Figs. 3b, 3d).
In 2013, the diet of 100% of whitefish was based on
Daphnia magna, up to 95% of the total composition of
organisms found in the gastrointestinal tract, among
which cyanobacteria and filamentous diatoms of the
genus Melosira were present; in some specimens,
Cyclops abyssorum and solitary imagoes of chirono-
mids (Orthocladiinae) were found. In 2018, only 42%
of whitefish exclusively fed on planktonic organisms
and 37% on benthic organisms, while 21% of speci-
mens had both groups of animals in their intestines. In
2018, planktonic organisms in the bolus of whitefish
were represented by Cyclops sp. and Daphnia sp.; ben-
thic organisms, by larvae of chironomids, dragonflies
and mayflies, and mollusks of the genus Pisidium, but,
mainly, by amphipods (representatives of the family
Gammaridae). By 2018, amphipods were recorded in
MS to a depth of 50 m, where their abundance was
120 ind./m2; it was higher at a depth of 30 m, to

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BIOLOGY BULLETIN Vol. 48 No. 8 2021
KRYLOV et al.
Table 2. Average (m ± SD) number of species (S), abundance (N1), biomass (B2), and the Shannon index (Н) of zooplankton in the pelagic zone in Malyi (MS) and
Bolshoi (BS) Sevan in July and October 2013 and 2018
1 In the numerator, thous. ind. /m3, and in the denominator, proportion (%) of the total zooplankton abundance; 2 in the numerator, g/m3, in the denominator, proportion (%) of the
total zooplankton biomass.
Parameter
July October
MS BS MS BS
2013a2018b2013c2018d2013e2018f2013g2018h
SRotifera 2.8 ± 0.7 4.6 ± 0.9 4.2 ± 1.0 4.8 ± 0.6 1.8 ± 0.3*f4.4 ± 1.5 2.3 ± 0.6*h6.0 ± 0.8
Copepoda 4.8 ± 0.7 6.0 ± 1.1 4.0 ± 0.3 5.2 ± 0.8 4.0 ± 0.4*b2.7 ± 0.2 4.0 ± 0.0*h2.0 ± 0.2
Cladocera 3.0 ± 0.0*b2.2 ± 0.2 3.4 ± 0.2*d2.0 ± 0.0 2.8 ± 0.3 2.5 ± 0.2*h2.4 ± 0.3*h1.1 ± 0.1
Total 10.6 ± 1.4 12.8 ± 1.7 11.6 ± 1.4 12.0 ± 0.7 8.6 ± 0.3 9.6 ± 1.7 8.7 ± 0.9 9.1 ± 0.9
NRotifera
Copepoda
Cladocera
Total 60.0 ± 14.4*b132.8 ± 41.0 53.2 ± 9.5*d193.2 ± 24.2 111.0 ± 29.5*f38.2 ± 11.0 98.1 ± 21.6*h23.1 ± 3.2
BRotifera
Copepoda
Cladocera
Total 11.9 ± 4.1 12.23 ± 4.19 7.96 ± 1.57 15.21 ± 6.10 12.06 ± 5.21*f0.600 ± 0.139 15.08 ± 6.88*h0.396 ± 0.114
Н, bit/ind. 1.02 ± 0.19*b2.67 ± 0.25 1.35 ± 0.07*d3.12 ± 0.15 2.23 ± 0.05*f2.70 ± 0.3 2.25 ± 0.1*h3.10 ± 0.2
b,c
b,c
1.3 0.2*
3.4 1.4*
±
±
d
31.8 7.2*
31.2 10.6
±
±
d
d
8.0 0.9*
15.8 1.3*
±
±
66.2 11.9
37.4 8.4
±
±
f
7.5 3.8
7.0 2.1*
±
±
11.7 6.1
22.2 7.8
±
±
h
h
4.3 0.8*
6.0 2.2*
±
±
7.1 1.1
32.3 4.4
±
±
b
41.4 9.0
71.1 2.8
±
±
45.4 15.1
33.9 6.5
±
±
d
35.4 6.3
66.7 3.2*
±
±
55.2 10.1
28.1 3.3
±
±
f
f
57.8 14.2*
55.3 4.5*
±
±
h
h
10.8 1.3*
35.0 5.9*
±
±
h
h
52.3 12.9*
53.5 3.2*
±
±
4.6 0.7
22.5 3.6
±
±
b,
с
17.4 5.8*
25.5 3.9
±
±
55.5 22.6
34.9 7.2
±
±
d
9.8 2.9*
17.5 3.1
±
±
71.9 23.4
34.5 6.9
±
±
f
45.6 14.6*
37.7 5.1
±
±
15.7 4.0
42.8 4.0
±
±
h
41.5 9.3*
40.5 4.5
±
±
11.4 2.7
45.3 4.3
±
±
b,c
c
0.001 0.0001*
0.03 0.02*
±
±
0.056 0.013
1.1 0.6
±
±
d
0.009 0.002*
0.14 0.03
±
±
0.073 0.008
1.0 0.4
±
±
f
0.002 0.0007
0.055 0.033*
±
±
0.006 0.003
0.8 0.3
±
±
h
0.0015 0.0003
0.108 0.099*
±
±
0.005 0.001
5.9 3.2
±
±
b
b
0.64 0.13*
9.1 4.4*
±
±
2.93 0.87
26.5 4.7
±
±
d
d
0.41 0.09*
5.9 0.9*
±
±
2.44 0.81
18.0 2.9
±
±
f
f
1.32 0.17*
22.5 8.8*
±
±
h
0.261 0.049*
45.2 3.2
±
±
1.15 0.46
16.2 8.9
±
±
0.095 0.031
29.0 6.8
±
±
b
11.2 4.1
90.8 4.4*
±
±
9.26 3.34
72.4 4.5
±
±
d
7.5 1.5
94.0 0.9*
±
±
12.69 5.39
81.0 3.0
±
±
f
f
10.74 5.12*
77.4 8.8*
±
±
0.333 0.089
54.1 3.1
±
±
h
h
13.93 6.51*
83.7 9.0*
±
±
0.296 0.113
65.1 7.5
±
±

BIOLOGY BULLETIN Vol. 48 No. 8 2021
FEATURES OF STRUCTURAL CHANGES IN THE PLANKTON COMMUNITY 1277
Table 3. Average (m±SD) abundance (N, thous. ind./m3), biomass (В, g/m3), and rate of mineral phosphorus excretion (Р,
gP/(m3 day)) by Daphnia longispina (I), Diaphanosoma lacustris (II), and Daphnia magna (III) in the pelagic zone of Malyi
(MS) and Bolshoi (BS) Sevan in July and October 2013 and 2018
Parameter
Species
July October
MS BS MS BS
2013а2018b2013c2018d2013e2018f2013g2018h
NI 13.6 ± 5.1*b31.4 ± 12.3 6.8 ± 2.5*d58.5 ± 16.5 0.2 ± 0.1 0.3 ± 0.1*h0 0.005 ± 0.004
II 2.0 ± 0.9*b24.1 ± 11.5 1.9 ± 0.4*d13.4 ± 8.1 42.3 ± 13.3*f15.2 ± 4.1 34.6 ± 6.5*h11.4 ± 2 .7
III 1.8 ± 0.9 0 1.1 ± 0.2 0 3.1 ± 1.4 0 6.9 ± 3.5 0
BI 3.9 ± 1.2 7.9 ± 3.1 3.0 ± 0.9*d12.0 ± 4.9 0.067 ± 0.063*f0.020 ± 0.013 0 0.0001 ± 0.0001
II 0.08 ± 0.04*b1.3 ± 0.5 0.08 ± 0.02 0.7 ± 0.6 1.52 ± 0.44*f0.312 ± 0.097 1.51 ± 0.31*h0.296 ± 0.113
III 7.3 ± 3.6 0 4.5 ± 0.7 0 9.16 ± 4.87 0 12.42 ± 6.28 0
PI0.131 ± 0.051*b0.337 ± 0.132 0.060 ± 0.024*d0.677 ± 0.174 0.0013 ± 0.001 0.004 ± 0.002*h00.00008 ±
0.00007
II 0.030 ± 0.013*b0.382 ± 0.193 0.028 ± 0.006*d0.224 ± 0.119 0.540 ± 0.185*f0.233 ± 0.062 0.416 ± 0.076*h0.188 ± 0.037
III 0.009 ± 0.005 0 0.006 ± 0.001 0 0.014 ± 0.006 0 0.034 ± 0.018 0
Total 0.170 ± 0.060*b0.720 ± 0.312 0.094 ± 0.028*d0.901 ± 0.274 0.556 ± 0.191*f0.237 ± 0.061 0.451 ± 0.089*h0.188 ± 0.037
560 ind./m2, and in BS, the density reached 60 ind./m2
at a depth of 25 m. In 2013, representatives of the fam-
ily Gammaridae were present only to a depth of 15 m,
where their average abundance was 60 ind./m2.
October. In 2018, the temperature was higher than
in 2013: in MS, by 0.5–2.3°С in the 0–30 m water col-
umn, and in BS, by 0.5–3.6°С from the surface to the
bottom (Table 1, Figs. 1а, 1b). In addition, a decrease
in the water transparency and oxygen deficiency in the
layer below 20 m was recorded in 2018 (Fig. 1c).
During both years of studies, no differences were
found in the phytoplankton biomass between MS and
BS; they were also absent between 2013 and 2018
(Table 1). The phytoplankton biomass was basically
formed by diatoms (from 75.2 to 86.7%). There were
also no differences in the quantitative characteristics
of bacteria between two parts of the lake (Table 1), but
in 2018, their abundance and biomass significantly
decreased in both parts of the lake compared to 2013.
In addition, the abundance and biomass of heterotro-
phic nanoflagellates was higher in 2018 than in 2013.
There were no differences in the specific number of
zooplankteur species between the parts of the lake
(Table 2). In 2018, the number of species of Rotifera
increased and that of Copepoda decreased in both
parts of the lake, while the number of Cladocera spe-
cies decreased in BS.
In 2013, the zooplankton abundance did not differ
between MS and BS, and in 2018, the density of
Copepoda and their proportion in the total abundance
were lower in BS (Table 2). The abundance was
formed by Copepoda in 2013 and by Cladocera in
2018. In 2013, nauplii of Copepoda, copepodites of
Calanoida, Acanthodiaptomus denticornis, Diaphаno-
soma lacustris, and Daphnia magna dominated in
terms of abundance. In 2018, Euchlanis dilatata,
Daphnia longispina, Diaphanosoma lacustris, and nau-
plii of Calanoida, dominated in MS, as well as
copepodites of Calanoida, while in BS, there were
Keratella quadrata, Filinia terminalis, and Cyclops
abyssorum. In 2018, the proportion of Rotifers
increased; the total abundance, abundance of Copep-
oda and Cladocera, and the proportion of Copepoda
in the total abundance decreased; and the Shannon
index value increased in both parts of the lake com-
pared to 2013 (Table 2).
The zooplankton biomass did not differ between
the two parts of the lake, only the biomass of Copep-
oda was higher in MS in 2018 (Table 2). In 2013,
Daphnia magna, Diaphаnosoma lacustris, and Acan-
thodiaptomus denticornis dominated in terms of abun-
dance in both parts of the lake; in 2018, Daphnia
longispina was dominant, in MS, and Diaphanosoma
lacustris and Acanthodiaptomus denticornis were also
present, and in BS, Cyclops abyssorum was. In 2018,
compared to 2013, the zooplankton biomass decreased
significantly due to crustaceans, the proportion of
Rotifera and Copepoda in the total biomass increased,
and the proportion of Cladocera decreased. In addi-
tion, in 2018, D. magna disappeared from the zoo-
plankton composition and the excretion of phospho-
rus by Cladocera decreased due to Diaphanosoma
lacustris in both parts of the lakes (Table 3).
The fish density in BS (2013, 92.9 ind./mln m3;
2018, 323.2 ind./mln m3) was higher than in MS (21.7
and 212.5 ind./mln m3, respectively). In 2013, the
main fish accumulations in MS were recorded in the
layers from 60 to 66 m (27.8%), from 25 to 35 m
(25.4%), and from 25 to 30 m (53.3%) (Figs. 2b, 2d).
They were to a greater extent concentrated and then
evenly distributed from a distance of ~1.5 km from the

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KRYLOV et al.
Fig. 2. The average proportion of f ish in their total abundance in the water column in (а, b) Malyi and (c, d) Bolshoi Sevan in (а, c) July 2013 and (b, d) October 2018.
70
50
45
40
35
30
25
20
15
5
10
55
60
65
010 20
Depth, m
%
2013
2018
70
50
45
40
35
30
25
20
15
5
10
55
60
65
010 20
Depth, m
%
35
30
25
20
15
5
10
010 20
Depth, m
%
35
30
25
20
15
5
10
010 20
Depth, m
%
(a) (b) (c) (d)

BIOLOGY BULLETIN Vol. 48 No. 8 2021
FEATURES OF STRUCTURAL CHANGES IN THE PLANKTON COMMUNITY 1279
shore (Fig. 4b). In 2013, the highest fish density in BS
was recorded in the layer of 24–30 m (53.0%); in 2018,
in the layers of 20–25 m (39.8%) and 7–10 m (30.6%)
(Figs. 2b, 2d), and the main accumulations were
recorded at depths of about 25 m at a distance of
~4 km from the shore (Fig. 4d).
In October 2013, the diet of 90% whitefish was
mainly composed of Daphnia magna; in 2018, only
28% of whitefish fed exclusively on planktonic organ-
isms (Calanoida), 44% on benthic organisms (mainly
representatives of the family Gammaridae), and 28%
of specimens had empty intestines.
DISCUSSION
The results of the study demonstrated that in some
years the differences in zooplankton characteristics
were found between the parts of the lake: the abun-
dance and biomass of Rotifera decreased and those of
Crustacea increased in MS where the fish density was
lower (Table 2). However, the most pronounced dif-
ferences in zooplankton at different fish density were
found when comparing the data of 2013 and 2018. At
the same time, some changes in zooplankton with an
increasing abundance of fish in 2018 were quite
expected (Hrbaček, 1962; Brooks and Dodson, 1965;
Stenson et al., 1978; Bartell and Kitchell, 1978; Gil-
yarov, 1987; Sadchikov, 2007). First, during that
period, D. magna, the largest and the most colored
species of Cladocera, disappeared from the composi-
tion of invertebrates. Second, a pattern was found that
was previously observed in Lake Sevan (Ozero Sevan
…, 2016): an increase in the Shannon index value. In
our opinion, the mechanism of changes in the index
value lies in the fact that fish, on one hand, select the
most visible food items and, on the other hand, can
switch to more numerous ones, regardless of their size
(Murdoch, 1969; Murdoch et al., 1975). At the same
time, grazing on both large and/or numerous organ-
isms contributes to a decrease in the degree of domi-
nance of one species in terms of biomass and/or abun-
dance, as a result of which the Shannon index value
increases.
However, some changes in plankton were rather
specific. Thus, the abundance and biomass of zoo-
plankton, including D. longispina and Diaphanosoma
lacustris, increased in the lake in July 2018 compared
to 2013 (Tables 2, 3). An obvious contradiction with
most literature data indicating that an enhanced pre-
dation pressure from planktivorous fish leads to a
decline in the abundance and biomass of zooplankton,
in particular, Cladocera (Hrbaček, 1962; Brooks and
Dodson, 1965; Stenson et al., 1978; Bartell and Kitch-
ell, 1978; Gilyarov, 1987; Sadchikov, 2007), raises the
question about the causes of the increase in the quan-
titative parameters of planktonic invertebrates in July.
The analysis of the intestinal content of whitefish
in 2018 showed that half of specimens fed only on ben-
thic forms (representatives of the family Gammari-
dae), whereas in 2013, 100% of specimens mainly fed
on Daphnia magna. It is obvious that the increase in
the abundance of whitefish with a benthic type of
feeding in 2018 was associated with a significant
increase in their abundance and, accordingly,
Fig. 3. Horizontal distribution of fish in (а, b) Malyi and (c, d) Bolshoi Sevan in (а, c) July 2013 and (b, d) 2018.
Distance from the shore, m
0
40
60
20
0 4000300020001000 5000 6000 7000
Depth, m
(a) 0
10
30
20
0 4000300020001000 5000 6000 7000
Depth, m
Distance from the shore, m
(c)
0
40
60
20
0 4000300020001000 5000 6000 7000
Depth, m
Distance from the shore, m
(b)
0
10
30
20
0 4000300020001000 5000 6000 7000
Depth, m
Distance from the shore, m
(d)

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BIOLOGY BULLETIN Vol. 48 No. 8 2021
KRYLOV et al.
increased competition for planktonic organisms
against the background of the disappearance of the
large D. magna. As a result, the fish density in the
deeper layers increased, especially at the depth dump
(about 20 m), where, apparently, fish fed on benthic
organisms.
Changes in the vertical distribution of whitefish in
July 2018 could have been caused by a high water tem-
perature (Table 1). It is known that fish can clearly dis-
criminate temperature gradients to the threshold of
0.1°С and choose the optimum temperature zone for
their physiological state (Steffel et al., 1976). Water
temperature is of particular importance for Coregonus
lavaretus, one of the most cold-loving fish species in
the modern ichthyofauna (Kudersky, 1997), which
prefers the hypolimnion in stratified lakes character-
ized by the most favorable temperature regime. How-
ever, even cold-loving fish such as C. lavaretus can
periodically move from the water layers with optimum
temperatures to less favorable layers that are rich in
food, when food is scarce (Brett, 1971; Smirnov,
2013). Thus, in 2013, when valuable food items of
whitefish such as amphipods were found only to the
depth of 15 m and the large Daphnia magna accessible
for whitefish was abundant in the water column, it was
easier for them to capture it in the upper layers of the
metalimnion and even in the lower layers of the
epilimnion. In 2018, when the composition of Cladoc-
era in the most heated layer of the epilimnion in July
included representatives of relatively small and
transluscent species, it became more beneficial for
whitefish to perform migrations to the hypolimnion
where their diet was composed of amphipods which
were recorded at depths to 50 m by that time. Conse-
quently, in 2018, fish chose the optimum combination
of temperature and trophic conditions which were
formed at a depth of about 20 m in the immediate
proximity of the bottom at the depth dump.
In addition, there is information that importance
of the top down control for zooplankton depends on
the trophic status of the water body: under better tro-
phic conditions, the effect of fish is less pronounced,
since grazing is compensated for by the higher fecun-
dity of invertebrates (Alimov, 2001). An increase in the
phytoplankton biomass in July 2018 compared to 2013
supports the idea of richer food resources of zooplank-
ton (Table 1).
However, an increase in the phytoplankton bio-
mass against increasing abundance and biomass of
zooplankton, including D. longispina and Diaphano-
soma lacustris, is rather uncommon. A higher water
temperature may have played a role in this, as evi-
denced by the correlation coefficients of the green
algae biomass (r = 0.59), cyanobacteria (r = 0.50), and
total phytoplankton biomass (r = 0.68).
In addition, the increase in the phytoplankton bio-
mass may be determined by the vital activity of zoo-
plankton filter feeders due to water enrichment with
their metabolites, which are nutrients for algae and
cyanobacteria (Zholtkevich et al., 2013). It is known
that the maximum rate of phosphorus excretion is typ-
ical for small-sized species of Cladocera (Ferrante,
1976). In 2018, the total biomass of relatively small-
sized Daphnia longispina and Diaphanosoma lacustris
Fig. 4. Horizontal distribution of fish in (а, b) Malyi and (c, d) Bolshoi Sevan in (а, c) October 2013 and (b, d) 2018.
0
10
30
20
0 4000300020001000 5000 6000 7000 8000
Depth, m
Distance from the shore, m
0
10
30
20
0 4000300020001000 5000 6000 7000
Depth, m
Distance from the shore, m
0
40
60
20
0 4000300020001000 5000 6000 7000
Depth, m
Distance from the shore, m
0
40
60
20
0 4000300020001000 5000 6000 7000
Depth, m
Distance from the shore, m
(a) (c)
(b) (d)

BIOLOGY BULLETIN Vol. 48 No. 8 2021
FEATURES OF STRUCTURAL CHANGES IN THE PLANKTON COMMUNITY 1281
significantly exceeded that in 2013; as a result, the
amount of excreted phosphorus increased: 4.2 times in
MS and 9.1 times in BS. Its quantity was positively cor-
related with the total phytoplankton biomass (r = 0.70).
Hence, phosphorus regenerated by Cladocera is
highly important for phytoplankton in Lake Sevan,
and along with a high water temperature, it stimulated
the growth of algae and cyanobacteria in July 2018,
thus supplementing their grazing and contributing to
the increase in their biomass.
Simultaneously, a decrease in the abundance and
biomass of bacterioplankton was recorded in July
2018. The studies of alpine lakes in Europe have shown
that only ~13% of variations of quantitative character-
istics of bacteria are explained by the direct effect of
zooplankton, in particular, by Daphnia (Straškrábová
et al., 2008). Some researchers believe that Daphnia
are not able to consume microorganisms of <1 μm
(Pace et al., 1983; Sanders et al., 1989). This, along
with the absence of a stimulating effect of excreted
phosphorus observed in Lake Constance (Gude,
1988) and in Lake Sevan in some periods (Krylov
et al., 2018), indicates an indirect effect of Cladocera
on bacterioplankton. It is known that large Daphnia
grazed mainly on protists, the main consumers of bac-
teria (Hall et al., 1993; Degans et al., 2002), in partic-
ular heterotrophic nanoflagellates. This is confirmed
by a number of observations showing that the quanti-
tative characteristics of heterotrophic nanoflagellates
in water bodies where small species of Cladocera pre-
vail are higher than in water bodies with large species
(Vaque and Pace, 1992; Krylov et al., 2018). This
explains the fact that in July 2018, when the large
Daphnia magna disappeared, the abundance of het-
erotrophic nanoflagellates in MS increased by 8.2
times and that in BS, by 10.7 times, with an increases in
the biomass by 6.1 and 6.3 times, respectively. The abun-
dance (r = –0.57 and –0.55) and biomass (r = –0.71 and
–0.55) of bacterioplankton decreased with an increas-
ing abundance and biomass of heterotrophic nanofla-
gellates. In addition, in July 2018, the proportion of
bacteria of >2 μm increased, which is known as a
defensive response of bacterioplankton against the
grazing pressure of its predators (Pernthaler, 2005).
When the water temperature dropped in October
2018, the fish control contributed to the decline in the
quantitative characteristics of zooplankton, including
Diaphanosoma lacustris and Daphnia longispina, and
the amount of phosphorus excreted by them (Tables 2,
3). This is indicated by the coefficients of correlation
between the total abundance and the biomass of zoo-
plankton (r = –0.78, –0.65, respectively), Copepoda
(r = –0.84, –0.82) and Cladocera (r = –0.71, –0.63)
and the fish density.
Significant grazing of zooplankton in October 2018
night have been not only due to the total increase in
the fish density but also to the patterns of their distri-
bution. It was previously shown that, in autumn,
whitef ish prefer deeper water layers (Smoley et al.,
1985; Gabrielyan, 2010). Similar data were obtained in
October 2013, when a relatively large fraction of fish
was recorded in the near-bottom areas (Figs. 2b, 2d).
However, in October 2018, they were concentrated in
shallower layers than in 2013. We explain this by the
low oxygen concentration in the near-bottom layers
(Fig. 1c). As a result, fish accumulations were
recorded at the horizons where both the temperature
(Figs. 1а, 1b) and oxygen conditions (Fig. 1c) were
optimal.
Therefore, the oxygen def iciency in the near bot-
tom layer (at depths more than 25 m) in October 2018
could have reduced the ability of the increased number
of fish to feed on benthic invertebrates due to which
planktonic crustaceans concentrated mainly in the
epi- and metalimnion (Ozero Sevan…, 2016) were
considerably consumed.
Interannual changes in the difference in the num-
ber of fish in MS and BS may also be hypoxia-related.
The highest density and biomass of fish were recorded
in BS, exceeding the values in MS by an average of 2–
4.8 times (Ekologia ozera …, 2010; Ozero Sevan …,
2016). The fish density in BS in July 2018 was higher
(by five times); in October 2013, by 4.3 times; but in
October 2018, only by 1.5 times. We assume that in
years with a critically low oxygen concentration in
near-bottom layers, fish migrate to MS, where the vol-
ume of the deep layer is larger than in BS. However,
this assumption requires particular studies.
Changes in zooplankton in October 2018 deter-
mined the state of other planktonic organisms. Thus,
an increase in the quantitative parameters of hetero-
trophic nanoflagellates was naturally associated with a
decrease in the top-down control of planktonic crus-
taceans (in the first turn, Daphnia magna), as evi-
denced by the correlation between the abundance of
protozoa and the abundance and biomass of Copep-
oda (r = –0.62 and –0.60) and Cladocera (r = –0.45
and –0.43), as well as by the literature data (Vaque and
Pace, 1992; Hall et al., 1993; Degans et al., 2002; Kry-
lov et al., 2018). In turn, the increase in the abundance
of heterotrophic nanof lagellates in October 2018 neg-
atively affected the abundance (r = –0.56) and bio-
mass (r = –0.48) of bacterioplankton.
A significant decline in the quantitative character-
istics of crustaceans, including filter feeders in Octo-
ber 2018, allows us to expect a decrease in their grazing
on phytoplankton and, as a result, an increase in its
biomass. However, the biomass of phytoplankton and
its structure practically did not change during that
period compared to 2013 (Table 1). Special attention
should be paid to the fact that this was observed
against the background of higher water temperature.
Apparently, as we mentioned above and earlier (Ozero
Sevan…, 2016; Krylov et al., 2016), phosphorus
excreted by Cladocera plays an important role in the
formation of plankton biomass, which is evidenced by

1282
BIOLOGY BULLETIN Vol. 48 No. 8 2021
KRYLOV et al.
the coefficient of correlation between its amount and
the phytoplankton biomass in October (r = 0.58). As a
result, when the amount of phosphorus regenerated by
Cladocera decreased, the phytoplankton biomass in
October 2018 was at the level of 2013.
CONCLUSIONS
Thus, as the density of the fish population
increases, changes in zooplankton and groups of
organisms controlled by it depend on the vertical dis-
tribution of planktophages determined by the water
temperature, oxygen concentration, and quantitative
characteristics of food items.
FUNDING
This study was supported by the Russian Foundation for
Basic Research (project no. 18-54-05003 Arm_а) and was
performed within the framework of a State Assignment
(project no s. А ААА-А18-11801269010 6-7, ААА А-А18-
118012690096-1, АААА-А18-118012690102-9, and АААА-
А18-118012690098-5).
COMPLIANCE WITH ETHICAL STANDARDS
Conf lict of interest. The authors declare that they have no
conflict of interest.
Statement on the welfare of animals. All applicable inter-
national, national, and/or institutional guidelines for the
care and use of animals were followed.
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Translated by N. Ruban