The planktonic Crustacean, represented by Cladocerans and Copepods, is an essential component of the trophic network of any waterbody (Dubovskaya 2009). Large Cladocerans (eg, genera Daphnia O.F. Müller, 1785, Simocephalus Schoedler, 1858) act as active filter feeders, playing a significant role in improving water quality and serving as food for fish (Bruce et al. 2006; Park, Shin 2007; Jeppesen et al. 2011; Mehner et al. 2016; Korponai et al. 2019; Gerasimova, Sadchikov 2021). Some copepods are intermediate hosts of parasitic infections, including those dangerous to humans (Zamora-Terol et al. 2021).
The main factor influencing the species richness of plankton communities, in addition to temperature, is mineralization (Zavarzin 2021; Anufriieva, Shadrin 2023) and the chemical composition of water (Krupa et al. 2008). With an increase in mineralization from the ultrafresh level to fresh and brackish waters, biological diversity increases, then decreases, and reaches a minimum at an indicator value of approximately 5-8 g/dm3 (Khlebovich 2013). As a rule, biological communities' species richness is higher in large waterbodies (Dodson 1991; Chertoprud et al. 2022) due to wider biotopic diversity in them compared to small ones.
The Balkhash-Alakol system includes five leading lakes (Balkhash, Alakol, Sasykkol, Koshkarkol and Zhalanashkol) located within the Balkhash-Alakol depression (Fig. 1). The largest of these is Balkhash Lake, with an area of 16,996 km² (Abrosov 1973). The Alakol (2,650 km²), Sasykkol (736,7 km²), Koshkarkol (120 km²) and Zhalanashkol (38 km²) lakes come after it (Filonets 1965). Sasykkol and Koshkarkol are flowing lakes, while the remaining lakes are endorheic. Water mineralization varies widely. The eastern Balkhash, Alakol, and Zhalanashkol with water mineralization ranging from 2.6 to 8.5 g/dm³ are saline, while the western part of the Balkhash, Sasykkol, and Koshkarkol lakes are fresh (Tarasov 1961; Amirgaliyev et al. 2003; Krupa et al. 2008).
Zooplankton studies of the Balkhash-Alakol lake system have been conducted for a long time (Samonov 1940; Malinovskaya 1959; Loginovskikh 1965; Loginovskikh, Dyusengaliev 1972; Dyusengaliev 1972; Abrosov 1973; Sharipova, Lopareva 1983; Mirabdullaev 1996; Sharapova 1999; Stuge 1999; Amirgaliyev et al. 2003; Stuge et al. 2004; Krupa et al. 2008; Krupa, Sharipova 2009; Krupa et al. 2013). Published articles mainly focus on the species composition and quantitative variables without distinguishing planktonic crustaceans as the community's leading group. This research, which aims to analyze the species richness and quantification of planktonic crustaceans, partially fills this gap.
Planktonic crustacean studies were conducted in the Balkhash-Alakol lake system between 2002 and 2007. Material was collected according to a station grid, depending on the water surface. In total, 441 samples were collected, including Balkhash – 169, Alakol – 150, Sasykkol – 69, Koshkarkol – 47, and Zhalanashkol – 9 samples. Zooplankton samples were collected using a small Juday plankton net with an input diameter of 12 cm by pulling it from the bottom to the surface. Filtered water was poured into 250 ml plastic containers. Samples were fixed with 40% formalin at a final concentration of 4%. Planktonic crustacean species were identified using guides (Rylov 1948; Manuilova 1964; Krupa et al. 2016). Zooplankton samples were processed using standard methods (Winberg, Lavrentieva 1984) with our modification. The sample was concentrated in a particular volume depending on the abundance of organisms. Usually, each sample was examined at several dilutions (250, 125, 50 ml), each time collecting 3 subsamples using a 1 ml pipette. Finally, the sample, with a volume of 20 to 25 ml, was examined as a whole. The step-by-step processing procedure allows a more accurate account of the species composition and the abundance of age stages. The results obtained were recalculated per 1 m³. Cluster analysis was performed using Primer 5 software, based on the Bray-Curtis index. Graphs and maps of sampling station locations in each of the lakes were plotted in R software, taking into account their coordinate reference.
In zooplankton, 74 species of planktonic crustaceans were found, including 48 species of Cladocera, 23 species of Cyclopoida, and 3 species of Calanoida (Table 1). Diaphanosomalacustris, Daphnia galeata, Mesocyclopsleuckarti, Thermocyclops crassus, and Arctodiaptomus salinus had the widest distribution. Ceriodaphnia reticulata, Chydorus sphaericus, Alona rectangula, Bosmina longirostris, and Leptodora kindtii were registered in the zooplankton of almost all lakes, but within their water areas, they occurred locally, mainly in the coastal zone.
Table 1. Species composition and frequency of occurrence of planktonic crustaceans in the Balkhash-Alakol lake system from 2002 to 2007
| Taxon name | Frequency of occurrence, % | ZK | Total | ||||||
|---|---|---|---|---|---|---|---|---|---|
| WB | EB | AK | SK | KK | ZK | Total | |||
| Sida cristallina (O.F. Müller, 1776) | 67 | 100 | 20 | - | 13 | - | 21 | ||
| Diaphanosoma brachyuran (Liévin, 1848) | - | 50 | - | - | - | - | 3 | ||
| Diaphanosoma dubium Manuilova, 1964 | - | - | 10 | - | - | - | 3 | ||
| Diaphanosoma lacustris Korinek, 1981 | 67 | 100 | 60 | 88 | 100 | 100 | 82 | ||
| Diaphanosoma macrophthalma Mirabdullaev, 1995 | 33 | - | 30 | - | - | - | 12 | ||
| Diaphanosoma mongolianum Ueno, 1938 | - | 50 | 30 | 13 | 25 | - | 21 | ||
| Diaphanosoma orghidani Negrea, 1982 | 67 | 50 | - | - | - | - | 9 | ||
| Daphnia pulex Leydig, 1860 | 33 | - | 10 | - | - | - | 6 | ||
| Daphnia longispina O.F. Müller, 1785 | - | 50 | 10 | - | - | - | 6 | ||
| Daphnia cucullata Sars, 1862 | 33 | 50 | - | - | - | - | 6 | ||
| Daphnia galeata Sars, 1863 | 67 | 100 | 80 | 100 | 13 | - | 62 | ||
| Simocephalus vetulus (O.F. Müller, 1776) | 33 | 50 | - | 13 | - | - | 9 | ||
| Simocephalus mixtus Sars, 1903 | - | 50 | - | - | - | - | 3 | ||
| Moina micrura Kurz, 1875 | - | - | 30 | - | - | - | 9 | ||
| Moina brachiata (Jurine, 1820) | - | - | 60 | - | - | - | 18 | ||
| Ceriodaphnia quadrangula (O.F. Müller, 1785) | - | 50 | 80 | - | 13 | - | 29 | ||
| Ceriodaphnia reticulata (Jurine, 1820) | 33 | 100 | 90 | - | - | 100 | 44 | ||
| Ceriodaphnia laticaudata P.E.Müller, 1867 | 33 | 100 | 20 | - | - | - | 15 | ||
| Ceriodaphnia pulchella Sars, 1862 | - | - | 10 | - | - | - | 3 | ||
| Ceriodaphnia setosa Matile, 1890 | - | - | 20 | - | - | - | 6 | ||
| Ceriodaphnia dubia Richard, 1894 | - | - | 20 | - | - | - | 6 | ||
| Macrothrix hirsuticornis Norman & Brady, 1867 | 33 | 50 | 20 | - | - | 33 | 15 | ||
| Macrothrix laticornis (Jurine, 1820) | - | 50 | 30 | - | - | 33 | 15 | ||
| Macrothrix spinosa King, 1853 | 33 | 50 | - | - | - | - | 6 | ||
| Macrothrix daday Daday, 1898 | - | - | 20 | - | - | - | 6 | ||
| Macrothrix triserialis Brady, 1886 | - | 50 | - | - | - | - | 3 | ||
| Ilyocryptus agilis Kurz, 1878 | 33 | - | - | - | 13 | - | 6 | ||
| Ilyocryptus acutifrons Sars, 1862 | 67 | - | - | - | - | - | 6 | ||
| Camptocercus rectirostris Schoedler, 1862 | 33 | 50 | 10 | 13 | - | - | 12 | ||
| Acroperus harpae (Baird, 1834) | 67 | 50 | - | - | - | - | 9 | ||
| Monospilus dispar Sars, 1862 | - | 50 | - | - | - | - | 3 | ||
| Graptoleberis testudinaria (Fischer, 1848) | 33 | 50 | 30 | - | 25 | - | 21 | ||
| Chydorus sphaericus (O.F. Müller, 1776) | 67 | 100 | 100 | 25 | 13 | 33 | 53 | ||
| Chydorus ovalis Kurz, 1875 | - | 50 | - | - | - | - | 3 | ||
| Pleuroxusaduncus (Jurine, 1820) | - | 50 | 20 | 13 | - | - | 12 | ||
| Pleuroxusun cinatus (Baird, 1850) | - | 50 | - | - | - | - | 3 | ||
| Pleuroxust rigonellus (O.F.Müller, 1776) | - | 100 | - | - | - | - | 6 | ||
| Alona costata Sars, 1862 | 33 | 100 | 10 | - | 13 | - | 15 | ||
| Alona guttata Sars, 1862 | 67 | 50 | 10 | - | 13 | - | 15 | ||
| Alona rectangula G.O.Sars, 1862 | 67 | 100 | 90 | 13 | 38 | - | 50 | ||
| Alonella nana (Baird, 1843) | 33 | 100 | - | - | 25 | - | 15 | ||
| Alonellaexigua (Lilljeborg, 1853) | - | - | - | - | 13 | - | 3 | ||
| Alonellaexcisa (Fischer, 1854) | - | - | - | 13 | - | - | 3 | ||
| Bosmina longirostris (O.F.Müller, 1776) | 67 | 50 | 80 | 25 | 13 | 33 | 44 | ||
| Polyphemus pediculus (Linnaeus, 1761) | - | 50 | 10 | - | 13 | - | 9 | ||
| Leptodorakindtii (Focke, 1844) | - | 100 | 10 | 25 | 25 | - | 21 | ||
| Scapholeberis kingi Sars, 1888 | - | - | 20 | 13 | - | - | 9 | ||
| Scapholeberis rammneri Dumont & Pensaert, 1983 | - | 50 | - | - | - | - | 3 | ||
| Cyclopoida | |||||||||
| Macrocyclops albidus (Jurine, 1820) | 33 | 100 | 10 | - | - | - | 12 | ||
| Eucyclops serrulatus (Fischer, 1851) | 33 | 100 | 50 | - | 13 | - | 26 | ||
| Eucyclops denticulatus (Graeter, 1903) | 33 | 100 | 10 | 13 | - | - | 15 | ||
| Eucyclops speratus (Lilljeborg, 1901) | - | 50 | - | - | - | - | 3 | ||
| Eucyclops macrurus Sars, 1863 | 33 | 50 | 20 | - | - | - | 12 | ||
| Paracyclops affinis Sars, 1863 | - | - | - | 13 | - | - | 3 | ||
| Paracyclops fimbriatus Fischer, 1853 | - | 50 | 10 | - | - | - | 6 | ||
| Ectocyclops phaleratus Koch, 1838 | - | - | 10 | - | - | - | 3 | ||
| Cyclops vicinus Uljanin, 1875 | 67 | 50 | 90 | - | 25 | - | 41 | ||
| Mesocyclops leuckarti Claus, 1857 | 67 | 100 | 100 | 100 | 100 | - | 88 | ||
| Mesocyclopsp epheiensis Hu, 1943 | 33 | 50 | - | - | - | - | 6 | ||
| Thermocyclops oithonoides (Sars G.O., 1863) | 33 | - | - | - | - | - | 3 | ||
| Thermocyclops dybowski Landé, 1890 | - | - | - | - | - | 33 | 3 | ||
| Thermocyclops rylovi (Smirnov, 1928) | - | - | 30 | - | - | - | 9 | ||
| Thermocyclops crassus (Fischer, 1853) | 67 | 100 | 80 | 100 | 100 | - | 82 | ||
| Thermocyclops taihokuensis Harada, 1931 | 67 | - | 60 | - | - | - | 24 | ||
| Thermocyclops vermife Lindberg, 1935 | - | - | 10 | - | - | - | 3 | ||
| Diacyclops bicuspidatus (Claus, 1857) | - | - | 10 | - | - | - | 3 | ||
| Diacyclops bisetosus (Rehberg, 1880) | - | - | 10 | - | - | - | 3 | ||
| Megacyclops viridis (Jurine, 1820) | - | 50 | 80 | - | - | 100 | 35 | ||
| Acanthocyclops robustus (Sars G.O., 1863) | 67 | 100 | 20 | - | - | - | 18 | ||
| Microcyclop safganicus Lindberg, 1948 | 33 | - | - | - | - | - | 3 | ||
| Microcyclops rubellus (Lilljeborg, 1901) | 33 | 50 | - | - | 13 | - | 9 | ||
| Calanoida | |||||||||
| Eurytemora affinis (Poppe, 1880) | 33 | - | - | - | - | - | 3 | ||
| Eudiaptomus graciloides (Lilljeborg, 1888) | - | - | - | 50 | 38 | - | 21 | ||
| Arctodiaptomus salinus (Daday, 1885) | 67 | 100 | 100 | 100 | 100 | 100 | 97 | ||
| Total | 38 | 48 | 47 | 18 | 23 | 9 | 74 | ||
Note: WB – West Balkhash, EB – East Balkhash, AK – Alakol, SK – Sasykkol, KK – Kossharkol, ZK – Zhalanashkol.
The results of the cluster analysis indicated that the lakes surveyed are divided into four distinct groups according to the species composition of planktonic crustaceans (Fig. 3). The first cluster covered the entire water body of Balkhash Lake, despite the notable differences in water mineralization between its western freshwater section and the eastern saline part. The key species characteristic of this group include the cladocerans Diaphanosoma orghidani, Daphnia cucullata, Macrothrix spinosa, Acroperus harpae, and copepod Mesocyclops pehpeiensis.
Zhalanashkol Lake formed a distinct cluster, demonstrating a low level of similarity to other lake communities. The characteristic species was Thermocyclops dybowski. In Alakol Lake, which represents the third cluster, zooplankton includes cladocerans Diaphanosoma dubium, Moina micrura, M. brachiata, Ceriodaphnia pulchella, C. setosa, C. dubia, and Macrothrix daday. Additionally, cyclopids such as Ectocyclops phaleratus, Thermocyclops rylovi, T. vermifer, Diacyclops bicuspidatus, and D. bisetosus were identified. The fourth cluster covers the freshwater Sasykkol and Kossharkol Lakes, with the characteristic species of Eudiaptomus graciloides.
Common species in all lakes except Zhalanashkol were Diaphanosoma lacustris, Daphnia galeata, Mesocyclops leuckarti, Thermocyclops crassus, and Arctodiaptomus salinus. In the Zhalanashkol Lake, Daphnia galeata and Mesocyclops leuckarti were absent, but Ceriodaphnia reticulata and Megacyclops viridis were widespread.
The abundance of planktonic crustaceans varied by orders of magnitude (Table 2). The highest values were recorded in the freshwater Zhalanashkol, Sasykkol and Koshkarkol lakes, and the lowest values were observed in the mineralized Balkhash and Alakol lakes.
Table 2. Mean annual abundance of planktonic crustaceans in the Balkhash-Alakol lake system
| Lake | Years | Abundance, ind. 103/m3 | |||
|---|---|---|---|---|---|
| Cladocera | Cyclopoida | Calanoida | Total | ||
| Balkhash | 2003–2004 | 12.1±2.8 | 15.1±1.6 | 19.7±2.2 | 46.8±4.8 |
| Alakol | 2002–2007 | 2.8±0.7 | 7.5±1.7 | 7.5 ± 2.3 | 17.8 ± 3.3 |
| Sasykkol | 2002, 2004–2007 | 41.5±17.8 | 23.1±5.5 | 25.0±8.3 | 89.6±30.4 |
| Koshkarkol | 2003–2007 | 23.8±11.4 | 28.8±13.4 | 20.6±6.1 | 73.2±29.1 |
| Zhalanashkol | 2005–2007 | 60.2±19.4 | 12.1±9.0 | 33.4±21.0 | 105.9±41.0 |
The interannual dynamics of planktonic crustaceans in the Sasykkol, Koshkarkol, and Alakol lakes were synchronous (Fig. 4), with Pearson’s correlation coefficient values of 0.828–0.925, p<0.05. In all lakes, the outbreak of plankton crustaceans was recorded in 2005, against the backdrop of rising water levels. In Zhalanashkol Lake, where the observations were conducted for only three years, a high community abundance (average 173.6 thousand ind./m3) was also observed in 2005. In 2006, the values decreased almost six times (31.8 thousand ind./m3), subsequently rising to 112.1 thousand ind./m3 in 2007. From 2003 to 2004, the abundance of planktonic crustaceans in the Western Balkhash increased on average from 36.2 to 59.3 and in the Eastern Balkhash from 44.0 to 47.6 thousand ind./m3.
During the examined period, cladocerans were the dominant group in terms of abundance in Zhalanashkol and Sasykkol lakes. On the contrary, cyclops or calanoids prevailed in the communities of the other lakes. The composition of the dominant complexes remained relatively constant and usually included 2 to 4 species (Table 3). The share of dominant species did not exceed 44.0% of the total abundance of crustaceans.
Table 3. Composition of dominant species of planktonic crustaceans in the Balkhash-Alakol lake system from 2002 to 2007
| Lake | Dominant Species | Abundance (%) |
|---|---|---|
| Alakol | Mesocyclops leuckarti | 26.1 |
| Arctodiaptomus salinus | 42.0 | |
| West Balkhash | Diaphanosoma lacustris | 23.4 |
| Mesocyclops leuckarti | 19.8 | |
| Thermocyclops crassus | 13.0 | |
| Arctodiaptomus salinus | 40.1 | |
| East Balkhash | Diaphanosoma lacustris | 19.5 |
| Mesocyclops leuckarti | 17.4 | |
| Thermocyclops crassus | 10.8 | |
| Arctodiaptomus salinus | 44.0 | |
| Zhalanashkol | Ceriodaphnia reticulata | 40.9 |
| Megacyclops viridis | 11.5 | |
| Arctodiaptomus salinus | 31.6 | |
| Koshkarkol | Diaphanosoma lacustris | 29.9 |
| Mesocyclops leuckarti | 15.0 | |
| Thermocyclops crassus | 23.7 | |
| Arctodiaptomus salinus | 26.6 | |
| Sasykkol | Diaphanosoma lacustris | 2.3 |
| Mesocyclops leuckarti | 26.1 | |
| Arctodiaptomus salinus | 42.0 |
During our research, 74 species of planktonic crustaceans were identified in the Balkhash-Alakol lake system, which is 19 species more than was previously known (Samonov 1940; Malinovskaya 1959; Loginovskikh 1965; Loginovskikh, Dyusengaliev 1972; Dyusengaliev 1972; Abrosov 1973; Sharipova, Lopareva 1983; Mirabdullaeav 1996; Sharapova 1999; Stuge 1999; Amirgaliyev et al. 2003; Stuge et al. 2004). The mineralized lakes Balkhash (57 in total) and Alakol (47) were characterized by the greatest species richness of the communities. This is due to their large area and the diversity of external conditions (Dodson 1991; Zavarzin 2021), including hydrochemical variables, and the removal of planktonic crustaceans with river runoff (Sharapova 1999).
Comparison with data from the literature (Stuge 1999; Stuge et al. 2004) showed that over the past decades the background species complex remained constant and included Diaphanosoma lacustris, Arctodiaptomus salinus, Thermocyclops crassus, and Mesocyclops leuckarti. The appearance of the cladoceran Daphnia magna, uncharacteristic for the waterbodies of the system (Sharipova, Lopareva 1983), in the late 1980s was associated with a high level of pollution in the lakes and an unfavorable hydrological regime (Stuge et al. 2004). During the same period, Eudiaptomus graciloides, previously common in freshwater lakes, disappeared from zooplankton. During our studies, it was again recorded in the Sasykkol and Koshkarkol Lakes, which may be associated with improved environmental conditions.
According to the results of the lake cluster analysis, the surveyed formed four clusters according to the species composition of planktonic crustaceans. The main factor in the differences in species composition is mineralization of the water, which varies on average from 0.4 to 0.6 g/dm3 in Sasykol and Koshkarkol to 4.6 to 7.8 g/dm3 in Alakol and the eastern Balkhash (Krupa 2012). Variability in hydrochemical conditions is also observed within the lakes’ water areas, from 1.2 to 2.2 g/dm3 in the zones of influence of river runoff to 5.9 g/dm3 in the eastern part of Balkhash and 9.2 g/dm3 in the deep water zone of Alakol. Despite the difference in hydrochemical conditions, the species composition of planktonic crustaceans in the West and East Balkhash is characterized by a high level of similarity. This is due to the high proportion of euryhaline species in the community and desalinated zones in the eastern mineralized part of the lake.
Freshwater lakes were characterized by a higher abundance of planktonic crustaceans (on average 73.2 to 104.9 thousand individuals/m3) than mineralized ones (17.8 to 45.8 thousand individuals/m3). In addition to trophic conditions and mineralization, one of the reasons for the differences identified in the abundance of planktonic crustaceans is the chemical composition of the water. The water in the Alkakol and Balkhash lakes contains a large amount of alkali metal ions (Krupa et al. 2008; 2010), which is unfavorable for most species of aquatic organisms.
The synchronous dynamics of planktonic crustaceans in three interconnected lakes (Alakol, Sasykkol, and Koshkarkol), with a maximum in 2005, reflected the influence of natural and climatic factors, in particular, interannual fluctuations in the water level. The maximum abundance of planktonic crustaceans in Zhalanashkol, isolated from other lakes in the system, was also observed in the high-water year 2005. This indicated that the influx of nutrient compounds into lakes with surface runoff was greater than what was accumulated in the lakes. This pattern was previously shown for several water bodies in Kazakhstan, where wastewater is not discharged directly (Krupa 2012). In Lake Balkhash, which is polluted by municipal and industrial wastewater discharges, as well as the influx of polluted runoff from the Ili River, the relationship between the long-term dynamics of the abundance of zooplankton (without isolating planktonic crustaceans) and the level of water was weakly expressed (Krupa, Sharipova 2009; Krupa et al. 2013).
The planktonic crustaceans of the Balkhash-Alakol lake system were represented by 74 species, of which 48 are Cladocera, 23 are Cyclopoida and 3 are Calanoida. Diaphanosoma lacustris, Daphnia galeata, Chydorus sphaericus, Alona rectangula, Bosmina longirostris, Mesocyclops leuckarti, Thermocyclops crassus, and Arctodiaptomus salinus are the most common. The highest number of planktonic crustacean species was recorded in the mineralized lakes Balkhash and Alakol, while the total abundance was higher in the freshwater lakes. The differences in the species composition and quantitative variables of planktonic crustaceans were determined by several primary factors: the area of the lakes, the diversity of biotopes, the mineralization, and the chemical composition of the water. The results obtained contribute to understanding the structure of the plankton communities under the influence of external factors.
This research was funded by the Ministry of Science and Higher Education of the Republic of Kazakhstan, the Scientific Program "Cadastre of Wild Animals in the arid territories of the Balkhash-Alakol basin with an assessment of threats to their conservation and sustainable use (BR21882199)".