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Article
Unusual vertical distribution of zooplankton and fish in the pelagic zone of Lake Sevan during summer stratification
Mikhail I. Malin* , Svetlana M. Zhdanova , Dmitriy B. Kosolapov , Inga P. Malina , Natalya G. Kosolapova , Rimma Z. Sabitova , Alexandr V. Krylov
I.D. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok 109, Nekouz District, Yaroslavl Region, 152742 Russia
*mishuk@ibiw.ru
Received: 12.03.2021 Abstract. Previous studies in Lake Sevan during summer
Revised: 19.04.2021 stratification have shown that the highest zooplankton abundance
Accepted: 19.05.2021 and biomass was found at the lower boundary of the epilimnion.
Published online: 13.08.2021 At the same time, whitefish (Coregonus lavaretus), being main
planktivorous species in the lake, preferred the hypolimnion, DOI: 10.23859/estr-210312 but was leaving this layer if dissolved oxygen concentrations
UDC 574.583:591(282.247.441.821) decreased to 1-5 mg/L. The study was conducted in Bolshoy
Sevan (the southern part of Lake Sevan) on July 29-30, 2019. Translated by D.M. Martynova jhe vertical profiles of water temperature and dissolved oxygen
concentration, as well as distribution of major taxonomic groups of aquatic organisms were assessed four times a day: in the dark (night time), in the light (day time), and in twilight (morning and evening). Fish population density was assessed using a "Simrad EK80" echosounder. Vertical distribution of zooplankton and fish observed within the study period did not correspond to that described earlier. Maximal zooplankton biomass during the study was recorded in the hypolimnion, and minimal biomass, in the epilimnion. Most of fish (89-100%) located in the metalimnion. At night, about 10% of the fish population descended to the hypolimnion, despite the low dissolved oxygen concentrations found there (3.0-3.1 mg/L). At dawn, about 7% of the fish ascended to the epilimnion, reaching a 7-m depth, where the water temperature was 20.8 °C. The water temperature range preferred by most fish individuals varied during the observation period and did not correspond to previously reported ranges.
Keywords: bacterioplankton, heterotrophic nanoflagellates, whitefish, Coregonus lavaretus, epilimnion, metalimnion, hypolimnion, migration.
To cite this article. Malin, M.I. et al., 2021. Unusual vertical distribution of zooplankton and fish in the pelagic zone of Lake Sevan during summer stratification. Ecosystem Transformation 4 (3), 27-41. https://doi.org/10.23859/estr-210312
Introduction
The study of the vertical distribution of biota in a stratified water body provides the researcher with unique material, since the distribution pattern obtained is a result of interactions of aquatic organisms in pronounced heterogeneous environment. Meantime, the spatial maxima of abundance of particular groups of organisms are the indicators of the optimal combination of biotic and abiotic factors. In some cases, unusual pattern forms, which differs much from well-known regularities; this makes it possible to re-evaluate the role of a factor or a complex of factors that have preconditioned such a phenomenon.
Historically, in a stratified Lake Sevan, the highest quantitative indicators of zooplankton were recorded in the epilimnion, in particular, along its lower margin (Krylov et al., 2010, 2016; Nikogosyan, 1985; Simonyan, 1991). In addition, general regularities of the vertical distribution of fish are known for water bodies of similar type; the pelagic species of the Arctic origin attract here special attention. Facing with stratification, they tend to occupy water layer(s), where the temperature conditions are optimal for their state; the latter are most often observed below the thermocline (Poddubny and Malinin, 1988). Main planktivorous species inhabiting Lake Sevan, Coregonus lavaretus (Linnaeus, 1758), prefers quite low water temperatures in summer: 4-9 °C in the northern-western part of Lake Sevan (Maly (Small) Sevan) and 5-7 °C in its southern part (Bolshoy (Big) Sevan) (Malinin et al., 1984).
At the same time, attention must be paid to the cases of disbalance of the known regularities of the vertical distribution of aquatic organisms. This is especially true in recent years, characterized by high air temperatures, contributing to changing the temperature and oxygen regimes of deep-water lakes (Helland et al., 2007; Razlutskij et al., 2018). The last affects the state of fish species of the Arctic complex, their distribution pattern, and the density of schools (Krivopuskova et al., 2014; Krivopuskova and Sokolov, 2018). In the 1980s, the distribution of whitefish in Lake Sevan depended on the distribution of dissolved oxygen: as the last decreased down to 1-5 mg/L in the hypolimnion, whitefish left this zone (Poddubny and Malinin, 1988). A change in the population density of plankton-feeding fish causes a transformation of the species composition and quantitative indicators of planktonic invertebrates. This is evidenced by a number of alpine lakes studied, where various species of trout were acclimatized for recreational purposes; as a result, large species of invertebrates, in particular, representatives of the genus Daphnia, disappeared due to their consuming by fish (Fitzmaurice, 1979; Galbraith, 1967; Gliwicz et al., 2000). During the study of Lake Sevan in 20142017, it was found that as the number of whitefish increased, the abundance and biomass of planktonic
crustaceans decreased, mostly due to decreasing share of the large species Daphnia (Ctenodaphnia) magna Straus, 1820 (Krylov et al., 2019a, b). Alongside with a significant increase in fish population density in 2018, D. magna disappeared from the zooplankton community, but the total abundance and biomass of planktonic invertebrates increased, mostly due to other Cladocera, D. (Daphnia) hyalina Leydig.,1860 (Krylov et al., 2021). The distribution of whitefish is the main reason for the uncharacteristic transformation of planktonic invertebrate communities due to the disappearance of D. magna, i.e. due to the depletion of the food supply in the water column. Altogether, these resulted in maximum fish density at greater depths than observed in previous years, where temperature and trophic conditions were optimally balanced. At the same time, the food spectrum of whitefish changed, and benthic invertebrates, in particular, amphipods (representatives of the family Gammaridae), had a significant proportion, while earlier it was D. magna. However, here we do not analyze the vertical distribution of zooplankton, which makes these assumptions less convincing.
In addition, it is important to take into account diurnal changes in the vertical distribution of zooplankton. Most of the results obtained over more than a century of studies of diurnal vertical migrations (DVM) indicate the following pattern: the descent of zooplankton into the deep layers at dawn and rise to the surface in the evening (Kiselev, 1980; Rudyakov, 1986). DVM of zooplankton are highly variable and complex behavioral phenomenon that obviously cannot be explained by a single factor. Most often, DVM are considered as a result of the complex influence of a number of both abiotic (vertical temperature gradients, ultraviolet radiation, chemical composition of water) and biotic (predation, competition, vertical distribution of food) factors (Brooks and Dodson, 1965; De Meester et al., 1999; Gerritsen, 1982; Han and Straskraba, 1998; Lampert, 1989; Lampert et al., 2003; Larsson and Dodson, 1993; Loose and Dawidowicz, 1994; Ohman et al., 1983; Rhode et al., 2001; Ringelberg, 2010; Shapiro and Wright, 1984; Sih et al., 2000; Spaak and Hoekstra, 1997; Tartarotti et al., 1999; Williamson et al., 2011). It is also necessary to consider separately the features of the vertical distribution of plankton, which are the result of DVM (i.e., active movement up or down), and the distribution patterns formed under other factors (passive transfer with water masses (including horizontal transport), consumption by plankton-feeding species, etc.).
The study aims to analyze the relationship between the diurnal dynamics of the vertical distribution of zooplankton and the planktivorous fish Coregonus lavaretus in the pelagic zone of Lake Sevan during water stratification in summer.
Materials and methods
Lake Sevan (N 40°18.6' E 45°20.9' ) is located in the center of the eastern part of the Republic of Armenia at an altitude of 1,900 m above sea level. The lake consists of two parts: Maly (Small) Sevan (area ~322 km2, max. depth 82 m) and Bolshoy (Big) Sevan (area ~928 km2, max. depth 36 m), which are connected by a 5.5-km wide strait (Asatryan et al., 2016).
The sampling was carried out in Bolshoy Sevan on July 29-30, 2019, onboard the R/V "Gidrolog" (site N 40°24.1' E 45°27.3'), where preliminary hy-droacoustic survey revealed pelagic schools of fish identified as whitefish. The material was collected at different periods of the day, differing in light conditions: in the evening twilight (at sunset), in the dark (at night), in the morning at twilight (at dawn), and in the daytime (maximum illumination). The sampling site depth was 24-26 m, this difference was due to the bottom relief (slope).
The water temperature and the content of dissolved oxygen were determined every 1-m lag with a multiparameter probe "YSI ProPlus" before taking biological samples in order to determine the boundaries of epilimnion (EL), metalimnion (ML), and hypolimni-on (HL) in the water column. Bacterioplankton (BP), heterotrophic nanoflagellates (HNF), and zooplankton (ZP) were collected every 1 m with a Molchanov's 4-L water sampler; the samples from EL, ML, and HL were pooled as integral samples for each layer.
In order to quantify BP and HNF, integral water samples from EL, ML, and HL were fixed immediately after sampling with formalin to a final concentration of 1%; the formalin solution was pre-filtered through a membrane filter (0.2-^m pore diameter). The samples were stored in the dark at 4 °C and processed in the laboratory for a month. The abundance and size of BP and HNF were determined by epifluorescence microscopy using DAPI and primulin fluorochromes, respectively (Caron, 1983; Porter and Feig, 1980).
The water samples were filtered through a plankton net (64-^m mesh size) to collect zooplankton, and residuals were fixed with 4% formalin. Sample processing was carried out according to the standard technique (Rivier, 1975), the biomass was determined taking into account the size of the organisms (Balush-kina and Vinberg, 1979). The number of zooplankton species per sample, abundance, biomass, proportion of taxonomic groups, average individual mass of certain organisms (AIM) dominant species and their similarity were assessed; similarity was determined by the Shorygin index (Vainshtein, 1976).
The vertical distribution of fish was estimated by the hydroacoustic method (Simmonds and MacLen-nan, 2005) with a "Simrad EK80" echo sounder with a dual-frequency antenna ES38-18/200-18C (split beam at 38 kHz, single beam at 200 kHz, 18° beam-width at both frequencies), the antenna was set at
1-m depth from the water surface. The survey was performed during the approach of the vessel to the sampling site. The distribution of fish was analyzed using the "Echoview 10" software by echo counting in the depth range from 2.5 m down to the bottom.
Results
The water temperature in the EL was 6.1-10.0 °C higher than in the ML and by 13.1-14.1 °C higher than in the HL (Fig. 1). During the day, it changed by 0.3-0.7 °C in EL, by 0.2-3.5 °C in ML, the maximum values were recorded at sunset and at night. In the HL, the water temperature fluctuated by 0.1-0.8 °C with the highest value registered at dawn. The minimum concentration of dissolved oxygen was found in HL, it was higher by 1.1-2.8 mg/L in ML, and by another 1.5-3.5 mg/L in EL (Fig. 1). During the day, its concentration varied by 0.1-0.2 mg/L in EL, by 0.91.9 mg/L in ML, and by 0.3-0.4 mg/L in HL; the maximum values were recorded at sunset and at night.
The position of the conditional boundary between EL and ML during the day changed by 2-3 m vertically, while the boundary between ML and HL was more stable and remained at a depth of 22-23 m (Fig. 1). In EL and ML, a decrease in water temperature was observed, most noticeable in ML, where the oxygen concentration also decreased. The dynamics of these characteristics has no daily cyclicity; it cannot be explained by the cooling of the water surface at night. This observation evidences indirectly on the presence of horizontal transfer of water masses (currents), which is most intense in the ML.
In EL, the minimum number of BP was found at dawn, in ML, at night and at dawn, in HL, during the day and at night; its increase in the entire water column was observed at sunset (Table 1). The cell volume and bacterial biomass in all water layers reached a minimum at night, while the maximum in EL and ML was noted during the day, and in HL, at dusk and dawn.
The maximum quantitative indicators of HNF in EL and ML were recorded at sunset and at night, in HL, at night and during the day (Table 1). Small flagellates (size > 5 ^m) made most of the population at that time. The minimum abundance and biomass of HNF in EL was found at dawn, in ML, during daytime; in HL, the greatest decrease in abundance was observed in the daytime, in biomass, at dawn. A decrease in the volume of flagellate cells in EL was recorded during the day, in ML, during the day and at night, in HL, at dawn. As a rule, at this time, the maximum share of small-sized forms (< 5 ^m) in the total abundance and biomass of HNF was observed.
Zooplankton was presented by seven species of Rotifera (Euchlanis dilatatа Ehrenberg, 1832; E. lyra Hudson, 1886; Filinia terminalis (Plate, 1886); Hexarthra mira (Hudson, 1871); Keratella quadrata (Müller, 1786); Polyarthra longiremis Carlin, 1943;
Table 1. Abundance (N), volume (V), and biomass (B) of bacterioplankton and heterotrophic nanoflagellates.
Bacterioplankton
Heterotrophic nanoflagellates
Light conditions
N, 3 ce mL
103 cells/ ,
V,
^m3
В,
mg/m3
N,
103 cells/ V, ^m3 mL
В,
mg/m3
< 5 ^m
N, % В, %
> 5 ^m
N, % В, %
Epilimnion
Dusk 5341 0.15 775 961 95.1 91.4 33.3 16.9 66.7 83.1
Night 5027 0.12 624 1068 61.9 66.1 30.0 17.4 70.0 82.6
Dawn 4595 0.17 786 420 63.0 26.5 50.0 16.8 50.0 83.2
Daytime 5027 0.28 1389 961 51.5 49.5 66.7 39.0 33.3 61.1
Metalimnion
Dusk 5341 0.14 751 1410 104.2 146.8 27.3 13.3 72.7 86.7
Night 4280 0.14 605 1495 51.4 76.9 78.6 48.8 21.4 51.2
Dawn 4241 0.18 774 1175 62.3 73.2 63.6 25.7 36.4 74.3
Daytime 5184 0.20 1022 961 57.6 55.4 55.6 41.6 44.4 58.4
Hypolimnion
Dusk 8090 0.22 1778 534 58.9 31.4 60.0 60.1 40.0 39.9
Night 5851 0.12 731 748 66.0 49.3 57.1 34.4 42.9 65.6
Dawn 6676 0.24 1624 540 43.9 23.7 67.8 51.9 17.0 32.9
Daytime 5144 0.19 963 427 122.5 52.3 0.0 0.0 100.0 100.0
Fig. 1. Vertical distribution of fish at dusk (A), in the night (B), at dawn (C), during the daytime (D) in epilimnion (EL), metalimnion (ML), and hypolimnion (HL). Upper X-axis: 1 - dissolved oxygen concentration, mg/L; 2 - water temperature, °C; lower X-axis: relative fish population density, %.
Synchaeta pectinatа Ehrenberg, 1832), four species of Copepoda (Cyclops abyssorum Sars, 1863; Diacyclops bicuspidatus (Claus, 1857); Acanthodi-aptomus denticornis Wierzejski, 1887; Arctodiapto-mus (Rhabdodiaptomus) bacillifer (Koelbel, 1885)), and three species of Cladocera (Daphnia hyalina; Diaphanosoma lacustris Korinek, 1981; Leydigia ley-digii (Schodler, 1863)). The number of species per sample varied insignificantly during the day, with the greatest change in ML and HL (Cv = 22.8 and 22.0, respectively), the lowest, in EL (Cv = 9.1) (Table 2). During the day and at sunset, the maximum number of species was found in EL, at night, in EL and ML, at dawn, in ML and HL. In EL, rotifers were always presented by the greatest number of species; in ML, they prevailed at sunset and at night, during the day the proportion of species of all taxonomic groups was the same, and rotifers and copepods prevailed at sunrise. In HL, during the day and at sunrise, Roti-fera also dominated by the species number, at sunset, these were Rotifera and Copepoda, at night, the proportion of species of all groups was equal.
The highest abundance of ZP at sunset and at night was observed in HL; during the day, the differences were insignificant, however, the lowest abundance was recorded in the ML, at dawn, in the HL (Table 2). The minimum range of abundance fluctuation during the day was observed in EL (on average, 1.2 times; Cv = 16.4), the maximum, in HL (on average, 1.8 times; Cv = 31.5), all noticeable changes occurred at sunset and at night, when population density increased in ML and HL, but decreased in EL. Copepoda brought the most of ZP in EL, replaced by Cladocera only at sunrise. The latter prevailed in ML at sunset and at night, in HL, during the entire observation period (Table 2). Keratella quadrata (except for the daytime in HL) and Daphnia hyalina (except for EL during the daytime, at sunset, and at dawn) were the dominant species in all layers of the water column during the day; in HL, their share in the total abundance was the largest (Table 3). Diaphanosoma lacustris dominated during the day in EL, at night and at dawn in ML, at dusk and dawn in HL; its largest share in the total number of ZP was observed in EL. Calanoida nauplii were dominants in EL, as well as in ML during the day and at dawn. The smallest similarity between the dominant species in EL and ML was recorded at sunset (21.7%), during the rest of the day, it varied within 32.9-44.6%. The minimum similarity of dominants was also noted during the day between the ML and HL (29.2%), the maximum, at sunset (56.0%), at the rest of the time, it was 43.3% and 48.4%. During the day, the dominant species common to the EL and HL layers were absent; however, the similarity increased up to 33.6% at sunset; during the rest of the day, it was 16.2% (at night) and 23.7% (at sunrise).
The highest ZP biomass during the day was recorded in HL, the lowest, in EL (Table 2). Fluctuations of biomass in EL were insignificant (on average, 1.1 times; Cv = 9.8), in ML they were more pronounced (on average, 1.6 times; Cv = 33.6), reaching maximum in HL (on average, 2 times; Cv = 42.7). In ML and HL, an increase in biomass was observed at sunset and at night due to crustaceans, and the minimum values were noted during the day. Cladocera prevailed, their biomass decreased during the day in the entire water column, the maximum values were recorded in EL at sunset and dawn, in ML and HL, at night (Table 2). The highest biomass of Copepoda in EL was recorded during the day, in ML, at dawn, in HL, at night; the lowest values were observed in EL at dawn, in ML and HL, during the day. In all layers and at any time of the day, Daphnia hyalina dominated, its largest share was always characteristic for ML and HL, the lowest share, in EL, especially during the day (Table 3). Diaphanosoma lacustris dominated only in EL (except for sunset), with the largest proportion observed during the day. Copepoda dominants were presented by Arctodiaptomus bacillifer (day and night in EL), as well as by Cyclops abyssorum (during the day in EL and ML, at dawn, in ML). Since Daphnia hyalina was one of the dominant species in terms of biomass in almost all samples, the indices of the similarity of dominants between different water layers were high (63.0-86.6%). However, in the daytime, due to a significant decrease in the proportion of D. hyalina in EL, the index of similarity with ML was 24.7%, with HL, 13.9%.
The maximum AIM of ZP organisms during the day was observed in HL, where the lowest values were noted during the daytime, the highest, at dawn (Fig. 2A). In ML, the minimum values were recorded during the day and at dawn, the maximum, at sunset. In EL, the variation of this indicator was low (Cv = 14.1), comparing to ML (Cv = 27.4) and HL (Cv = 23.7), the smallest value was noted at sunrise. Significant fluctuations in the AIM of the main dominant species, D. hyalina, were found in EL (Cv = 50.3), where it decreased during the day and at night, and increased at dusk and dawn (Fig. 2B). In HL, in the period from daytime to dawn, AIM of Daphnia increased (Cv = 36.4), reaching at dawn higher values than in other layers. In the ML, the AIM of Daphnia varied insignificantly (Cv = 18.1) with a maximum at sunset and at night, and a minimum in the daytime and at dawn. AIM of Diaphanosoma la-custris in EL was also characterized by a high degree of variation (Cv = 92.2); during the daytime, the highest value was noted, then it sharply decreased to lower values than in other layers (Fig. 2C). In ML and HL, the individual weight of D. lacustris varied to a lesser extent (Cv = 39.6 and 23.6, respectively); in HL it was lower; there were no differences only at night. AIM of Cyclops abyssorum also varied to the
Table 2. Number of species, abundance, biomass, and proportion of taxonomic groups of zooplankton in epilimnion (EL), metalimnion (ML), and hypolimnion (GL).
Taxonomic
Light
Number of species
Abundance, 103 ind./m3
Biomass, mg/m3
group conditions EL ML HL EL ML HL EL ML HL
Dusk 50.0 42.9 37.5 26.8 27.3 26.5 1.0 0.3 0.3
Rotifera, % Night Dawn 44.4 55.6 44.4 40.0 33.3 40.0 17.0 25.7 24.1 28.8 20.3 17.0 0.7 1.3 0.4 0.6 0.2 0.3
Daytime 50.0 33.3 50.0 31.2 15.2 8.3 1.1 0.3 0.1
Dusk 30.0 28.6 37.5 50.9 30.4 19.4 17.0 12.1 8.1
Copepoda, % Night 33.3 33.3 33.3 43.1 33.9 30.6 25.9 7.4 13.9
Dawn 22.2 40.0 30.0 32.9 40.8 30.4 12.9 21.5 11.7
Daytime 25.0 33.3 33.3 44.6 49.2 23.9 40.0 15.0 14.4
Dusk 20.0 28.6 25.0 22.3 42.3 54.1 82.0 87.6 91.6
Cladocera, % Night 22.2 22.2 33.3 39.9 42.0 49.1 73.3 92.3 85.9
Dawn 22.2 20.0 30.0 41.4 30.4 52.6 85.8 77.9 88.0
Daytime 25.0 33.3 33.3 24.2 35.6 67.8 58.8 84.6 85.5
Dusk 10 7 8 23.9 19.4 30.3 586.1 1244.3 2057.5
Total Night Dawn 9 9 9 10 6 10 18.2 27.5 30.8 27.8 41.6 20.7 465.2 516.3 1684.7 1034.2 3160.6 1723.8
Daytime 8 6 7 24.0 19.9 24.2 500.4 744.9 1109.5
greatest extent in EL (Cv = 79.8), comparing to ML (Cv = 32.9) and HL (Cv = 47.9); its maximum values during the day exceeded those in ML and HL (Fig. 2D). At sunset and at night, the individual mass of C. abyssorum decreased in EL, at sunrise, it slightly increased, but was lower than that in ML and HL, where the highest values were found at sunrise. AIM of Arctodiaptomus bacillifer in EL also had a greater degree of variation (Cv = 57.1) than in ML (Cv = 18.6) and in HL (Cv = 34.1) with a maximum during the day and a minimum at sunset (Fig. 2E). In the ML, the highest AIM of A. bacillifer was recorded at sunset; it decreased at night, and increased again at sunrise. In HL, the maximum was observed at night; during the rest of the time, the differences were insignificant, with a minimum observed at sunset. AIM of Copepo-
da juveniles was characterized by minimal variation in EL (Cv = 20.6), it was slightly higher in ML and HL (Cv = 36.8 and 36.5, respectively). The individual mass of nauplii and copepodites decreased at sunset in EL and HL, at sunrise and at night in ML, but increased at sunset in ML, at night in EL and HL and at sunrise in HL (Fig. 2F).
The average density of the spatial distribution of fish, calculated over the entire water column, varied during the day. The maximum value was recorded at night, the minimum, during the day, when the density decreased by 18 times, probably because of horizontal migrations to adjacent parts of the reservoir (Table 4). The fish preferred ML, where 89-100% of the population kept at different times of the day. At sunset, the maximum fish distribution density was found
-EL---ML ..........HL
Fig. 2. Average individual mass of key Zooplankton organisms: A - all the species; B - Daphnia hyalina, C - Diaphanosoma lacustris, D - Cyclops abyssorum, E - Arctodiaptomus bacillifer, F - juvenile Copepoda at dusk (I), in the night (II), at dawn (III), during the daytime (IV) in epilimnion (EL), metalimnion (ML), and hypolimnion (HL).
at an 18-m depth, where the water temperature was 15.4 °C; fish was absent in EL and HL (Fig. 1A). At night, the distribution of fish within the ML became more uniform, when the maximum density of their distribution was observed at a 19-m depth, where the water temperature was 11.6 °C. Less than 1% of the fish was recorded in the lower margin of EL, directly at the border with the ML; 10% of the fish descended to HL, where it was evenly distributed from the boundary with the ML to the bottom, despite the low oxygen content of 3.0-3.1 mg/L at a temperature of 6.9 °C (Fig. 1B). At dawn, fish were absent in the HL and were distributed over the entire ML layer, forming a maximum density at an 18-m depth at a temperature of 17.2 °C. In the lower and middle layers of EL, where the temperature reached 20.8 °C, 7% of the fish ascended (Fig. 1C). During the day, about 95% of the fish was concentrated in the ML, the maximum was observed at a 17-m depth at a temperature of 16.3 °C. Less than 1% of fish were recorded in HL and less than 5%, in EL (Fig. 1D).
Discussion
Studies performed in July 2019 evidenced on uncharacteristic vertical distribution of zooplankton for Lake Sevan during the day. First, attention is drawn to the minimum values of biomass in EL with maximum values in HL, as well as relatively low indices of the total ZP abundance. At the same time, there were no abiotic factors responsible such a distribution: the water temperature and the content of dissolved oxygen in HL did not correspond to the optimal conditions for the ZP development.
The influence of fish, which vertical distribution was also characterized by a number of atypical features, may be one of the reasons for the specific distribution of ZP; in many respects, our results did not agree with the previous data on Lake Sevan. Thus, it has been previously reported that whitefish prefer HL (Poddub-ny and Malinin, 1988) and leave it only if the oxygen concentration decreases down to 1-5 mg/L (Malinin et al., 1984). According to our observations, regardless of the time of day, most of whitefish keep in ML, while
Table 3. Composition and proportion of Zooplankton species dominating by abundance and biomass in epilimnion (EL), metalimnion (ML), and hypolimnion (GL).
Taxon EL Dusk ML HL EL Night ML HL EL Dawn ML HL Daytime EL ML HL
Share by abundance, %
Keratella quadrata 23.2 21.7 23.7 15.0 20.4 18.2 22.2 24.8 12.9 24.2 14.0 -
Daphnia hyalina - 34.3 44.0 16.2 30.2 39.5 - 20.0 40.9 - 29.2 58.7
Diaphanosoma lacustris 13.0 - 10.2 23.7 11.8 - 32.3 10.4 10.8 18.9 - -
Nauplii of Calanoida 19.5 - - 16.2 - - 17.2 12.0 - 18.9 22.9 -
Nauplii of Cyclopoida 14.9 - - - - - - - - - - -
Share by biomass, %
Daphnia hyalina 76.1 86.6 89.0 63.0 89.1 84.1 66.7 73.8 84.6 13.9 83.6 82.6
Diaphanosoma lacustris - - - 10.4 - - 19.3 - - 44.9 - -
Cyclops abyssorum - - - - - - - 13.4 - 14.4 10.8 -
Arctodiaptomus bacillifer - - - 13.3 - - - - - 17.5 - -
Table 4. Absolute spatial population density (D) and relative abundance (N) of fish in epilimnion (EL), metalimnion (ML), and hypolimnion (GL) and in the entire water column at different light conditions.
Water layer Dusk D, ind./106 m3 N, % Night D, ind./106 m3 N, % Dawn D, ind./106 m3 N, % Daytime D, inmd3/106 N, %
EL 0 0 90.9 0.8 552.6 7.0 30.8 4.3
ML 1481.5 100 10091.4 89.2 7351.9 93.0 678.8 94.9
HL 0 0 1134.3 10.0 0 0 5.5 0.8
Entire water column 740.7 - 5130.7 - 3765.8 - 279.8 -
at night up to 10% of them descend to HL, despite the low oxygen content in this layer (3.0-3.1 mg/L).
It has been also indicated that whitefish in Lake Sevan perform DVM, rising at night towards surface, when presumably following the food objects (Pod-dubny and Malinin, 1988). On the contrary, our observations evidence that at nighttime about 10% of the fish descends from ML to HL, and some fish ascent from ML to EL (7%), where they are recorded at dawn (Figs. 1 B, 1 C).
The preferred water temperatures, which may be tracked by the depth of maximum fish density, also go beyond the ranges indicated earlier, i.e. 4-9 °C in Maly Sevan and 5-7 °C in Bolshoy Sevan (Poddubny and Malinin, 1988). In our study, the water temperature, preferred by most of the fish, changes during the day and does not fall into these ranges, when the whitefish prefers the coldest waters (11.6 °C) at night, and the warmest (17.2 °C) - at dawn, when, in turn, some fish ascend to EL, reaching a 7-m depth and a temperature of 20.8 °C (Fig. 1).
At the same time, the observed pattern of the white-fish distribution may be explained by the concept of choosing the energetically optimal environmental temperature under stratification conditions, proposed by a number of authors. At low temperatures in HL, metabolic processes slow down, which affects not only the duration of food digestion, but also the energy requirements of fish in general (Krogius, 1974; Poddubny and Malinin, 1988). Consequently, in the 1980s, the white-fish chose the cold-water HL, probably due to the lack of food resources, since its abundance in those years was much higher than nowadays (Gabrielyan, 2010).
Currently, only a small proportion of whitefish migrate to the HL, and only at night, most likely, to slow down metabolism and to conserve energy. The low oxygen content in the HL does not limit these migrations, since the oxygen demand also decrease, probably, as a result of the slowing down of metabolic processes. At night, whitefish practically does not feed (Poddubny and Malinin, 1988), which may explain the high abundance of ZP in HL. The ascend of a part of the fish school from ML to EL, observed at dawn, is probably also caused by ceasing of the feeding on ZP in the dark and due to a significant increase in the intensity of feeding in the morning. Presumably, at sunset, upon reaching the level of illumination of the water column, similar to that during dawn, the feeding intensity of whitefish increases as well, accompanied by partial migration to the EL, which has not been recorded in this study. A similar behavior was noted in the European vendace (Coregonus albula (Linnaeus, 1758)) in Lake Pleshcheyevo (Yaroslavl Region, Russia), based on the results of earlier original observations (Poddubny and Malinin, 1988).
Analysis of the spatiotemporal changes in fish population density in EL shows that during their maxi-
mum density at dawn (Table 4), some ZP parameters were higher than during the absence of fish at sunset (total abundance of ZP, Cladocera abundance, the abundance and biomass of Diaphanosoma lacustris and Arctodiaptomus bacillifer). At the same time, at the highest fish density, a decrease in the abundance and biomass of Copepoda, biomass of Cladocera, total biomass of ZP, biomass and average individual mass of Daphnia hyalina have been noted (Table 2, Fig. 2). In ML, the abundance and biomass of main taxonomic groups of ZP, D. hyalina, and Diaphanosoma lacustris, as well as their AIM at the maximum fish density was higher than at the minimum (Table 2, Fig. 2). In HL, at the highest fish density, the highest abundance and biomass of ZP and dominant crustaceans were also found, and AIM of Daphnia hyalina, Diaphanosoma lacustris, and Cyclops abysso-rum in this period was lower only when comparing to that at dawn (Table 2, Fig. 2). Consequently, only in EL, where most of the time the fish density and quantitative characteristics of ZP were lower than in other layers, a number of changes in the quantitative composition of invertebrates were observed. The latter are justifiably explained by the influence of fish nutrition in a number of publications (Hansson et al., 2007; Luecke et al., 1990; Mehner, 2000). However, in general, no noticeable effect on the ZP of spatiotemporal changes in fish density was revealed in the water column.
It is possible that the fish density increased due to their migration to the layers, where the abundance and biomass of the ZP increased, primarily of the dominant crustaceans, due to their daily migrations. It is known that crustaceans prefer deeper layers during the day and migrate to the upper layers at night, avoiding predators (Field and Prepas, 1997; Ringelberg, 2010; Stich, 1989). However, despite the most pronounced variation in the abundance and biomass of ZP in HL at the maximum at sunset and at night, we can state that during the period of our observations there were no clearly pronounced vertical migrations of the dominant crustacean species; their abundance, biomass, and the average individual mass changed simultaneously in all layers of water, regardless of the time of day or fluctuations in fish density.
Generally, this picture is not entirely consistent with most of the literature data, which indicate the persistence of diurnal migrations even in fishless mountain water bodies (Williamson et al., 2001). The absence of DVM in planktonic animals was recorded during hypoxia in HL, when most animals were found in EL (Doubek et al., 2018). In Lacamas Lake (USA), no DVM of zooplankton were recorded, but some taxa kept in layers with pronounced hypoxia (Nolan et al., 2019). On the other hand, it has been shown that certain species and groups of planktonic animals in different water bodies may have different characteris-
tics of DVM (Gladyshev, 1990), being both migrants and non-migrants. Some species can migrate within a water layer with certain temperature, for example, as Diaphanosoma mongolianum does within EL in Lake Pleshcheyevo (Zhdanova, 2018).
In Lake Sevan, relatively large (0.8-1.6 mm) Daphnia hyalina preferred HL and ML, and smaller (0.8-1.6 mm) Diaphanosoma lacustris was more often concentrated in EL (Fig. 2, Table 3). The confinement of species to certain layers of the water column was noted earlier in other water bodies (Karpowicz et al., 2020). In lakes Glubokoe (Moscow Region, Russia) and Pleshcheyevo (Yaroslavl Region, Russia), Daphnia cristata is confined to HL, D. galeata and D. hyalina, to ML, Diaphanosoma mongolianum and D. brachyurum, to EL (Stolbunova, 2006; Zhdanova, 2018; Zhdanova and Lazareva, 2009). In the water bodies of the canyon type in Czech Republic, Daphnia longispina and its hybrids more often dominated in ML and HL (Seda et al., 2007a). For D. galeata, genetically differentiated sub-populations have been identified, which do not leave the HL (Seda et al., 2007b).
Significant differences in the size of D. hyalina and Diaphanosoma lacustris precondition different filtration rates and food preferences of these species. It is known that the presence of fish stimulates the development of microscopic filter-feeders (Korov-chinsky, 2004). Consequently, in Lake Sevan, the presence of whitefish may positively affect the survival and reproduction of small-sized Diaphanosoma. These relatively small zooplankters are less susceptible to being grazed by fish, while the relatively large Daphnia are more vulnerable.
The changes in ZP may be caused by the horizontal transfer of organisms by the water currents (Armengol et al., 2012). In addition, the low quantitative characteristics of invertebrates in EL may be associated with the fact that the main share of potential fish food was observed here during the recorded morning and supposed evening ascent from the ML, as evidenced by the minimum AIM of ZP at this time. However, the greatest activity of fish in EL could occur during the daytime, as evidenced by the minimum biomass, by the share of one of the preferred food objects, Daphnia, in the total biomass and AIM, as well as by the absence of common dominant species in the EL and HL. Nevertheless, the fact of daytime activity of fish in EL has not been recorded by hydro-acoustic equipment; to confirm or refute this, continuous surveys are required.
The fish descended to HL only at night, despite the low oxygen content, which was not critical for invertebrates either. Some authors report that planktonic invertebrates, in particular, representatives of the genera Daphnia and Bosmina, can inhabit the lower layers of the water column even at low oxygen content and use them as refugia from predators, even
if the food source there is limited (Hanazato, 1992, 1995; Sell, 1998; Vanderploeg et al., 2009). Data on chlorophyll a, obtained only in the daytime unfortunately, also testify to the rich food base of the ZP in HL. Thus, in EL, its average amount was 0.6 ^g/L, in ML, 0.4 ^g/L, and in HL, 1.1 ^g/L. A sufficient food supply for ZP in HL is also supported by the quantitative composition of BP and HNF (Table 1). The average daily number and biomass of bacteria in HL were higher than that in EL and ML. It was found that the biomass of BP decreased as the abundance and biomass of HNF increased (rS = -0.63 and -0.62, p < 0.05); the average abundance and biomass of latter were lower in HL than in EL and ML. Probably, this was due to the control of their number by the ZP, which was indicated by the positive correlation between the biomass of invertebrates and the abundance of BP (rS = 0.58, p < 0.05).
We assume that the processes of horizontal transfer of ZP by currents and horizontal migrations of whitefish, which may help to explain some peculiarities of the dynamics of the observed characteristics, cannot cause directly such atypical features of the vertical distribution of the considered groups of aquatic organisms. Since these processes occur in a horizontal direction, organisms are not redistributed between EL, ML and HL. Horizontal transfer of water masses and horizontal migrations of fish played a certain role in the earlier stages of the reservoir's history, including the period of describing "typical" patterns of distribution of ZP and fish, but the role of horizontal transfer has not been studied.
Apparently, in this study, we observed the diurnal dynamics of rare patterns of the vertical distribution of whitefish and ZP, which were not described for Lake Sevan earlier. Possible reasons causing these patterns may be divided into two groups: (1) such changes did not occur during the periods of earlier observations, or (2) they did occur, but were not recorded. In the first case, the manifestation of new features of vertical distribution in two groups of aquatic organisms at once indicates changes in the ecosystem of the reservoir. They may be caused by a rise in the water level of the lake, significant fluctuations in the abundance of whitefish, changes in the species composition of zooplankton, phytoplankton blooms, as well as other phenomena occurring in Lake Sevan in recent decades (Krylov et al., 2019a, 2019b, 2021). It is also probable that the observed patterns are characteristic of ZP and whitefish from Lake Sevan, not recorded by earlier studies, since they appeared at a certain combination of events and lasted shortly. It should be noted that detailed comprehensive studies of the diurnal dynamics of the vertical distribution of aquatic organisms in this water body were carried out for the first time. Elucidation of the true reasons of the observed phenomenon requires further research. An increase in
the sample size of the material collected according to the proposed method may bring statistically significant estimates of the studied characteristics during the water stratification in summer in Lake Sevan.
Conclusions
Information on the atypical distribution of whitefish in Lake Sevan obtained in the summer of 2019 forces us to take a fresh look at the role of hypolimnion in ecosystems of stratified water bodies. In the hypolimnion, maximal zooplankton biomass may be observed, while the planktivore periodically migrates to the hypolimnion despite unfavorable oxygen conditions and does not exploit the available food resource, but uses the environmental conditions optimal for body energetics.
Our results evidence that assessing generally accepted factors preconditioning the daily dynamics of the vertical distribution of zooplankton, namely, presence of DVM of zooplankton against the background of the DVM of the planktivorous fish, cannot provide an unambiguous explanation of the study results. The observed site of the lake is an open system, where a continuous exchange of water mass with the rest of the reservoir takes place. For this reason, the environmental hydrophysical parameters change; due to passive transfer, zooplankton community changes as well, this makes it difficult to distinguish such processes from the consequences of DVM or consumption by planktivore, since fish are able to migrate horizontally back and forth to adjacent areas of the reservoir. Probably, all these changes are not characterized by a pronounced daily cyclicity.
Acknowledgments
The authors are grateful to A.I. Tsvetkov (I.D. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences) for measuring and providing hydrophysical data (water temperature, concentration of oxygen content) and assistance in collecting hydrobiological material. Special thanks go to G.A. Gevorgyan (Scientific Center of Zoology and Hydroecology of the National Academy of Sciences of the Republic of Armenia) for data courtesy (chlorophyll concentration) in Lake Sevan during the study period.
Funding
The study was carried out within the state assignments nos. AAAA-A18-118012690106-7, AAAA-A18-118012690102-9 and AAAA-A18118012690098-5.
ORCID
M.I. Malin 0000-0001-5513-6405
S.M. Zhdanova 0000-0003-1094-2010
D.B. Kosolapov 0000-0001-6854-0423
I.P. Malina 0000-0002-4257-2133
N.G. Kosolapova 0000-0002-2044-160X
R.Z. Sabitova 0000-0002-1558-7380 A.V. Krylov 0000-0003-1371-7310
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