Checklist and Distribution of Calanoida (Crustacea: Copepoda) in Kazakhstan (Central Asia)

: This work aims to analyze the zoogeographic distribution of Calanoida in Kazakhstan. Kazakhstan belongs to the Palaearctic region, and its territory is ascribed to the European–Siberian and Nagorno–Asian biogeographical subregions. The European–Siberian subregion includes the Volga–Ural, Irtysh, and Turkestan–Aral provinces. The Balkhash diversity of Calanoida in Kazakhstan. Calanoida fauna of Kazakhstan was closest to the fauna of countries with a continental climate and most strongly differed from countries with subtropical and Mediterranean types of climates.


Introduction
Calanoida is the most ancient group of aquatic invertebrates and plays an essential role in transferring energy from lower to higher trophic levels [1][2][3][4]. About 2000 Calanoida species are known in the world fauna, of which 610 species inhabit continental water bodies [4,5]. The distribution of the number of species among individual families of the order is not known precisely. For example, within Diaptomidae from 449 [6] to 515 species [7], within Centropagidae from 79 to 81 species. The lack of accurate data on the species richness and zoogeographic distribution of Calanoida [6,7] is associated with insufficient knowledge of the fauna of certain regions [8], ongoing description of new species [9][10][11][12][13], as well as invasions of species out of their natural distribution ranges.
The purpose of this work is to analyze the composition of the Calanoida fauna and the zoogeographic distribution of the species on the territory of Kazakhstan based both on unpublished records of species registered between 1997 and 2019, and verified occurrences reported in the works [9,23,24].

Study Site Description
The climate of most parts of Kazakhstan is continental, arid, and semi-arid, with cold winters and hot summers [25]. The average annual sunshine duration is 2000-3000 h. The average annual air temperature is +5.5 • C. In the southern parts, it reaches +15.8 • C. Most of the territory is characterized by a huge difference between the maximum (up to +42 • C) and minimum air temperatures (up to −57.2 • C). In most of the territory, the average annual precipitation reaches 100-500 mm, in the north of the country-350-650 mm, in mountainous areas up to 900-1200 mm. Most of the rainfall occurs in spring and early summer. The driest months are July and August. In mountainous areas, precipitation falls all year round.
The climatic features of the territory cause high temperatures of waters (up to 24-32 • C in summer), mostly high Total Dissolved Solids (TDS) values (more than 0.3-0.5 mg/dm 3 ), and low alkaline to alkaline water properties [23]. Ultra-fresh and freshwater bodies are distributed mainly in the mountainous regions of South, South-East, and East Kazakhstan. A relatively low content of organic substances and nutrients is typical for the water bodies of Kazakhstan [26].
According to zoogeographic zoning [27], most Kazakhstan territory belongs to the Palaearctic zoogeographic region. The European-Siberian subregion is distinguished within its limits, divided into the Volga-Ural, Irtysh, and Turkestan-Aral provinces, and the Nagorno-Asian subregion, represented by the Balkhash province ( Figure 1).
The Volga-Ural province includes the basin of the Ural River and water bodies of western Kazakhstan. The hydrographic network is represented mainly by small rivers, permanent and temporary steppe lakes, and ponds, from ultra-fresh to salty waters. There are no large lakes and reservoirs, except for the brackish lake Shalkar with a water area of about 205.8 km 2 .
Irtysh province occupies a vast territory of Central, Eastern, and Northern Kazakhstan. It includes the basin of the Irtysh River in the east and the territory to the Ural River basin in the west. The largest water bodies are Zaysan and Markakol lakes and Bukhtarma reservoir. There are many small permanent and temporary lakes in the floodplain of the Irtysh River. Fresh and ultra-fresh water bodies prevail in the east. The TDS of water in water bodies in the northern and western parts of the province varies over a vast range-from 0.3 to 300 g/dm 3 .  Turkestan-Aral province includes the Syrdarya river basin and the Aral Sea. Many reservoirs have been created on the river and its tributaries, including Shardara, Badam, Tasotkel, Ters-Ashchibulak, and others. The TDS of water in the water bodies of the Syrdarya basin varies from 0.5 to 1.5 g/dm 3 , in the Aral Sea-from 9.0 to 23.0 g/dm 3 .
The Balkhash province unites mountainous regions and basins of the endorheic lakes Balkhash, Alakol, and the Chu, Talas, Ili rivers. In mountainous areas, ultra-fresh and fresh lakes and reservoirs, smaller in area, prevail. Plain lakes Balkhash and Alakol are characterized by an increased content of dissolved salts-from 1.1 to 8.9 g/dm 3 . In Sasykkol, Koshkarkol, and Zhalanashkol lakes, TDS water reaches 0.4-1.5 g/dm 3 .
The Ponto-Caspian brackish water area includes the Caspian Sea (except for the Kara-Bogaz-Gol Bay). The TDS values vary from 0.5-1.1 g/dm 3 in the zone of influence of the runoff of the Volga and Ural rivers to 9-12 g/dm 3 in the deep part of the Caspian Sea (Middle Caspian Sea).
Zooplankton samples were collected between 1997 and 2019 in 130 water bodies located in different regions of Kazakhstan ( Figure 1). The largest are the Caspian and Aral seas, lakes Balkhash, Alakol, Markakol, Sasykkol, Koshkarkol, Zhalanashkol, reservoirs Kapchagai, Shardara, Samarkan, Yntymak, Badam, and Sorbulak ( Table 1). Most of the surveyed water bodies have an area of less than 10 km 2 . In addition to lakes, reservoirs, and temporary reservoirs, samples were taken in the Syrdarya, Ili, Ural, Emba, and Nura rivers, as well as small rivers and springs. The water bodies are located at altitudes from −27 to 3170 m above sea level ( Table 2). The temperature of the surface water layers in summer varies from 14.9 to 32.0 • C. The total dissolved solids (TDS) in water vary widely. The lowest values of the indicator are typical for mountain lakes and reservoirs with glacial nutrition. A relatively increased TDS is recorded in the endorheic lowland lakes. In the north of the country, there are hyperhaline lakes; their water contains up to 100.0-350.0 g/dm 3 of total dissolved solids. Table 2. Types of the surveyed water bodies, their altitude above sea level, TDS, and maximum water temperature.

Taxon Sampling and Species Identification
Zooplankton samples were taken with a Juday plankton net (mesh size 64 µm), with a mouth diameter of 12 cm, by towing it from the bottom to the surface. The filtered water was poured into plastic containers with a volume of 250 mL. Samples were fixed with 40% formalin to a final concentration of 4%. At each water body, sampling of zooplankton was carried out according to a grid of stations, taking into account one station per 1.5-2.5 km 2 of the water surface. In small lakes and reservoirs, 3-5 samples were taken. In large water bodies, the number of collected zooplankton samples varied from 10 to 50. A total of 7250 zooplankton samples were collected and processed.

Statistical Analysis
We visualized the similarity in Calanoida fauna between different regions by build-ing a dendrogram based on the Bray-Curtis distance. Bray-Curtis Cluster Analysis was done using Primer 5 Software [37].

Results
The species composition of Calanoida in Kazakhstan is given in Table 3. Overall, that 26 species from 5 families and 18 genera are reliably known in the Calanoida fauna of Kazakhstan (Table 4). The largest number of Calanoida species was found in the Irtysh province ( Table 3 To date, only four species have been reliably recorded in the Ponto-Caspian region.    Only four species are widespread: Acanthodiaptomus denticornis, Arctodiaptomus (R.) salinus, Phyllodiaptomus blanci, and Eudiaptomus graciloides. The first species is recorded in mountainous ultra-fresh lakes and lowland water bodies, with a TDS of up to 0.5-1.1 g/dm 3 . A. (R.) salinus occurs in water bodies with a wide gradient of TDS (0.4-231.7 g/dm 3 ) and reaches its highest abundance at 4.2-18.0 g/dm 3 . P. blanci is found mainly in ponds and small lakes in South and Central Kazakhstan. E. graciloides is recorded both in mountainous ultra-fresh lakes and in lowland lakes and reservoirs and steppe lakes with relatively high water salinity.
According to the cluster analysis based on the values of the Bray-Curtis index (Figure 2), the similarity of species composition of more than 50% revealed only between Kazakhstan and two countries-Romania and Ukraine. About 45% of the species in the fauna of Kazakhstan were common with countries such as Israel, Turkey, Mongolia, and Uzbekistan. About 40% of the species identified in the fauna of Kazakhstan were also found in Russia and Europe. The Calanoida fauna of Kazakhstan was significantly different from the Calanoida fauna of China, Italy, Azerbaijan, Georgia, Armenia, Tajikistan, and Turkey.
Of the total number of species, five are non-native. Three of them (Sinodiaptomus (Sinodiaptomus) sarsi, Neutrodiaptomus (Neutrodiaptomus) incongruens, Neodiaptomus schmackeri are representatives of the Far Eastern complex [28]. S. (S.) sarsi and N. (N.) incongruens were found in the water bodies of the southern and southeastern parts of Kazakhstan more than 30 years ago [59]. N. schmackeri was first discovered in the Shardara reservoir (South Kazakhstan) in 2003 and 2007 [60]. Later it was recorded in the lower reaches of the Syrdarya River before its confluence with the Small Aral. This species of Calanoida most likely entered the water bodies of Kazakhstan with fish imported from the Far East [61]. In 1998 S. (S.) sarsi is indicated for Turkey [55] and in 2016 for Ukraine [50]. N. schmackeri entered Europe similarly due to the introduction of fish from Asia to Albania [36].
Calanipeda aquaedulcis and Acartia (Acanthacartia) tonsa entered the Caspian Sea from the Black Sea with the ballast waters of ships, respectively, in 1905 and 1981. In the 1950s, C. aquaedulcis was introduced into the Aral Sea to improve its food supply [61]; it survived the salinization of the Sea and is currently the dominant species in zooplankton. A. (A.) tonsa has long been mistakenly identified as A. (Acartiura) clausi [62]. Our long-term studies of the zooplankton of the Caspian Sea confirmed the occurrence of A. (A.) tonsa in it [58]. Confusion in the definition of these closely related species could arise in connection with the morphological variability of individuals. According to our studies, male A. (A.) tonsa from the northeastern Caspian Sea are distinguished by the presence of a small, rounded projection armed with a spine in the proximal part of the 2nd article of the fifth leg [63]. In individuals from the Middle Caspian, this protrusion is absent or weakly visible. In males of the closely related species A. (A.) clausi, the 2nd article of the right leg of the fifth pair has a large, rounded projection in the distal part.
Endemic species Eurytemora caspica [13], Gigantodiaptomus irtyshensis [10], and Arctodiaptomus (Arctodiaptomus) naurzumensis [9] are still known only from typical habitats: the northern part of the Caspian Sea, a small lake in the floodplain of Irtysh river (East Kazakhstan) and Naurzum lakes (North Kazakhstan). Eight more species are also rare. Diaptomus (Chaetodiaptomus) mirus, Eudiaptomus transylvanicus, Arctodiaptomus (Arctodiaptomus) dentifer, and Arctodiaptomus (Rhabdodiaptomus) ulomskyi were found in small steppe water bodies of western Kazakhstan on the border with Russia. The invader Neodiaptomus schmackeri is known from the Syrdarya River and Shardara reservoir. According to our data [64], Eurytemora affinis is mainly found in the basin of the Nura River (Central Kazakhstan), less often in the middle reaches of the Irtysh River. Metadiaptomus asiaticus inhabits water bodies of Northern and Eastern Kazakhstan with TDS of 5.9-343.3 g/dm 3 [45]. We found Arctodiaptomus (Rhabdodiaptomus) bacillifer only in a small floodplain lake situated in Lake Balkhash basin. Repeated indications of the finding of this species in water bodies of Kazakhstan with high TDS require confirmation since it is often confused with A. (R.) salinus and A. (R.) acutilobatus [64].
The composition of the Calanoida fauna is determined by regional climatic conditions that affect the density of the hydrographic network, temperature, and water salinity. The arid climate of most of Kazakhstan determines the occurrence of a significantly smaller number of water bodies compared to humid zones. The predominance of euryecious or euryhaline Calanoida species, adapted to changing external conditions, is associated with pronounced fluctuations in temperature and TDS of water in Kazakhstan [65].
In addition to paleoclimatic factors [66], the distribution of the species' richness of Calanoida by zoogeographic provinces reflects the regional and climatic features of various regions of Kazakhstan. The density of the river network and the number of water bodies connected with rivers is one of the factors in the formation of the species' richness of the fauna of arid territories [67]. The largest number of Calanoida species in the Irtysh province (Table 3) is due to the good water supply in the territory, various climate types, and types of aquatic ecosystems. Most of the water bodies, primarily fresh, are concentrated in the eastern part of its territory. In the northern region, in addition to fresh and brackish lakes, there are many hyperhaline lakes. The central part has the smallest number of water bodies, among which the Korgalzhyn lakes are the most significant, with a water salinity of 1.1-154.6 g/dm 3 [68]. More impoverished fauna in other zoogeographic provinces is associated with poor water resources.
The originally poor composition and originality of the fauna of the Ponto-Caspian region are associated with its complex origin and the specific chemical composition of the water of the Caspian Sea. Currently, only four species have been reliably recorded here, including the invasive species Acartia (Acanthacartia) tonsa and Calanipeda aquaedulcis, the autochthonous Heterocope caspia [69], and endemic species Eurytemora caspica [13]. As mentioned above, three autochthonous species (Limnocalanus macrurus, Eurytemora grimmi, Eurytemora minor) have not been recorded in the zooplankton of the Caspian Sea for several decades. In addition to the negative influence of the ctenophore Mnemiopsis leidyi [57], their disappearance may be due to competitive displacement by the more eurybiontic invaders Acartia and Calanipeda.
According to cluster analysis (Figure 2), over 50% of common species have been identified for Kazakhstan, Romania, and Ukraine; about 45% of common species with Israel, Turkey, Mongolia, and Uzbekistan; about 40% of species are found in Russia and European countries (including the European part of Russia). Kazakhstan Calanoida was characterized by a low level of similarity with countries such as China, Italy, Azerbaijan, Georgia, Armenia, Tajikistan, and Turkey. The results obtained are associated with both the climatic features of the compared territories and with a different degree of knowledge of the fauna of the order in different countries.
As can be seen from Table 5, the Calanoida fauna of Kazakhstan was closest to the fauna of countries with a continental climate and most strongly differed from countries with subtropical and Mediterranean climates. Comparison of our results is difficult due to the lack of complete lists of Calanoida species for Azerbaijan, Georgia, Armenia, and Tajikistan.

Conclusions
There are 26 species of Calanoida registered in Kazakhstan. A comparison of the pattern of species diversity showed that the richest in species composition (20) is the Calanoida fauna of the Irtysh province. In the Volga-Ural province, ten species were recorded, in the Turkestan-Aral province-eight, in the Balkhash province-seven, and in the Ponto-Caspian region-six. Acanthodiaptomus denticornis, Arctodiaptomus (Rhabdodiaptomus) salinus, Phyllodiaptomus blanci and Eudiaptomus graciloides are found everywhere. Five species are invaders. Far Eastern Sinodiaptomus (Sinodiaptomus) sarsi, Neutrodiaptomus (Neutrodiaptomus) incongruens, Neodiaptomus schmackeri entered Kazakhstan, most likely with fish; Acartia (Acanthacartia) tonsa and Calanipeda aquaedulcis-with ships' ballast water. Along with Mnemiopsis leydyi, the copepods that entered the Caspian Sea could contribute to the extinction of the autochthonous species Limnocalanus macrurus, Eurytemora grimmi, and Eurytemora minor. Eurytemora caspica, Gigantodiaptomus irtyshensis, Arctodiaptomus (Arctodiaptomus) naurzumensis, Diaptomus (Chaetodiaptomus) mirus, Eudiaptomus transylvanicus, Arctodiaptomus (A.) dentifer are currently known to have a limited area of distribution. The description of endemic Calanoida species and the species new for the region, mainly from small water bodies, testifies the important role of this category of water bodies in maintaining biological diversity. The results obtained contribute to the knowledge of the Calanoida fauna of regions with a continental climate. The revealed similarities and differences of the Calanoida fauna are associated both with the climatic features of the compared territories and with a different degree of knowledge of the fauna of the order in different countries.