Copepods play an important ecological role in aquatic ecosystems. They occupy different ecological niches in aquatic food webs, contribute to biological element cycles, and transfer organic matter from primary producers to higher secondary consumers(Fenchel, 1988; Frangoulis et al., 2004). Copepods also have the potential to control malaria and dengue by consuming mosquito larvae(Marten et al., 2000), and they are intermediate hosts of many fi sh and bird parasites(Monchenko, 2003). 21 000 species of copepods are known; they dwell in marine and continental aquatic habitats(Walter and Boxshall, 2015). A small number of copepod species have adapted to an existence in hypersaline waters(i.e. those with salinity >35×10^-3)(Bayly and Boxshall, 2009; Shadrin, 2012; Anufriieva, 2014). Hypersaline systems are not only one of harshest environments on Earth(Grant, 2004), but they also usually undergo dramatic salinity variations(Belmonte et al., 2012; Shadrin, 2012). Hypersaline lakes and lagoons provide home for many bird species nesting and wintering there and also provide seasonal settlement for many thous and s of migrating birds. Copepods are among the main food items for many of them. Copepods are used in aquaculture. The question is therefore asked whether copepods inhabit hypersaline waters worldwide, and if so, what are their specific properties of copepods provide this.

This paper summarizes the published data on copepods inhabiting hypersaline waters worldwide and discusses some of their eco-physiological and biogeographical features enabling them to exist in such harsh and unpredictable variable environments as hypersaline water bodies.

We studied copepods in hypersaline waters of the Crimea, the largest peninsula in the Black Sea with over 50 hypersaline lakes of both marine and continental origin(Shadrin, 2009). Those lakes are shallow, polymictic, and vary in size, biota and have a range of fluctuating abiotic factors. At least 13 copepod species inhabit them(Tseeb, 1958; Kolesnikova et al., 2008; Zagorodnyaya et al., 2008; Balushkina et al., 2009; Belmonte et al., 2012; Anufriieva, 2014; Anufriieva et al., 2014). This Crimean extreme environment is not an exception: copepod species dwell in hypersaline waters worldwide. Table 1 show that there are at least 26 copepod species around the world that can exist at salinity higher than 100 g/L; among which 12 species are found at salinities exceeding 200 g/L. In the Crimea, Cletocamptus retrogressus Shmankevitch, 1875 was found at 360 g/L(with density of 1 320 individuals/m ³) and Arctodiaptomus salinus Daday, 1885 at 300 g/L(with density of 343 individuals/m ³). Probably those species are the most halotolerant copepods in the world(Table 1). Some unidentifi ed cyclopoid species were also twice found at salinities higher than 300 g/L in two regions of Tibet of China(Zhao et al., 2005) and in the Shanxi Province(our unpublished data).

Table 1 Copepod species in hypersaline waters worldwide

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High salt concentration is toxic for most organisms because the salt greatly reduces the availability of water, a requirement for life(Grant, 2004). Thus, halophiles and halotolerant organisms have evolved highly specialized physiological adaptations for maintaining a proper osmotic balance in such a hostile environment. Aquatic organisms with various salt tolerances adapt to their environments through osmoregulation and osmoconformation(Khlebovich and Aladin, 2010). Osmoregulators tightly regulate the osmolarity in the body at a constant level. Osmoregulators, such as the anostracan Artemia, actively control salt concentrations despite the high and fluctuating salt concentrations in the environment. The osmoconformers do not possess mechanisms at the organismal level to regulate the solutes in their body fluids at a concentration different from that in the external medium. Osmotic adaptation therefore may occur at the cellular level by increasing the intracellular concentration of organic compatible osmolytes(small organic molecules), which are either synthesized in the cell or transported into it from the external environment(Imhoff, 1986; Yancey, 2001). Many different small molecules are known to serve as organic osmolytes and other compatible solutes. These solutes fall into a few major chemical categories: small carbohydrates including sugars, polyols and derivatives; amino acids and derivatives; methylamines and methylsulfonium compounds(Yancey, 2001). Such use of osmolytes is widespread, having been reported from Archaea to mammalian tissues such as kidney and brain(Yancey, 2001). Animalosmoсonformers of different taxa also solve the problem in the same way(Yancey, 2001; De Vooys and Geenevasen, 2002; Seibel and Walsh, 2002). Many copepods are osmoconformers(Bayly and Boxshall, 2009; Svetlichny et al., 2012). Synthesis and increased concentration of free amino acids(alanine, proline and glycine)during acclimation to high salinity have been observed in two orders of copepods, Harpacticoida and Calanoida(Burton, 1991; Van Der Meeren et al., 2008; Lindley et al., 2011). Free amino acids are often used, but they are not only one type of osmolytes in copepods; other types of osmolytes also present in copepod cells(Goolish and Burton, 1989). The cells of some extremely salinity-tolerant invertebrate species use intracellular organic osmolytes which are quite different from the free amino acids usually encountered in less euryhaline species(Pierce et al., 1984). Some arthropods(e.g. larvae of Culex tarsalis Coquillett, 1896)may use different types of osmolytes, such as the amino acid proline and the disaccharide trehalose, and accumulate the exogenous osmolyte sorbitol(Patrick and Bradley, 2000).

Life of all organisms at high salt concentrations is energetically expensive. An upper salt concentration limit, in which every organism can live, is determined to a large extent by bioenergetic constraints(Oren, 2011). The main factors that determine whether a certain type of organism can live at high salinity are the amount of energy generated during its dissimilatory metabolism and the amount of energy needed for osmotic adaptation. As an example, the highlyhalotolerant unicellular green alga Dunaliella synthesizes glycerol in response to salinity stress; its content in the cell is proportional to the medium salinity and can reach 80% of the dry weight(Ben- Amotz et al., 1982; Chen and Jiang, 2009). The harpacticoid copepod Tigriopus californicus(Baker, 1912), when transferred from water with a salinity of 17×10^-3 into sea water(salinity 35×10^-3), uses up to 23% of its total energy expenditure to increase the synthesis of free amino acids(Goolish and Burton, 1989). The energy expenditure for the synthesis of osmolytes at much higher salinity would be much larger for copepods; it is clear that the species is unlikely to meet its energy needs at salinity above 70–100 g/L(Shadrin and Anufriieva, 2013). The species cannot survive if it is forced to synthesize the osmolytes itself, but it can take them up from the environment. An exoosmolyte hypothesis was suggested(Shadrin and Anufriieva, 2013): high halotolerance in osmoconforming copepods is determined by exoosmolyte consumption mainly with food. All previous observations of A . salinus and C . retrogressus at very high salinity in lakes of the Crimea occurred during intense blooms of the green algae Dunaliella with concentrations reaching 6×10 ⁷ cells/L and 60 g/m ³(Senicheva, 2005; Senicheva et al., 2008; Anufriieva and Shadrin, 2012; Anufriieva, 2014); as a result the water in the reservoirs had a redorange color. The halotolerant Apocyclops cf. dengizicus(Lepeshkin, 1900)was also recorded at extremely high salinity levels during a cyanobacterial bloom(Carrasco and Perissinotto, 2012); cyanobacteria may synthesize different osmolytes under high salinity(Imhoff, 1986; Oren, 2011). Therefore it is logical to suggest that in these conditions A . salinus, C . retrogressus, and A . cf. dengizicus as well as other copepods may obtain their osmolytes from feeding on Dunaliella or cyanobacteria, and perhaps also absorbing them from dissolved organic matter. Therefore they do not need to spend energy resources to maintain the necessary level of osmolytes in their cells. It was shown in experiments with A . salinus that copepods in vessels with microalgae blooms can live at higher salinity than in vessels with lower microalgae concentrations(Anufriieva and Shadrin, 2014a).

The halotolerance range of copepods— osmoconformers is not determined solely by the physiological peculiarity of the species. The salinity ranges of the species in natural water bodies show both physiological and ecosystem limitations. From the ecosystem point of view it is important to emphasize that osmolytes are ‘common property’ in a community. Many organisms readily transport the osmolytes from the environment into the cells; this gives them their resistance to osmotic stress, and is primarily typical for unicellular organisms(Zavarzin, 2003). When discussing the physiological capabilities of the copepod species to live in different environments, we must not overlook a community/ ecosystem metabolism as a whole. Further targeted experiments are needed to confi rm or disprove the hypothesis.

The geographic distribution of a small part of the highly halotolerant copepods is restricted to Australia(Calamoecia trilobata Halse and McRae, 2001, Meridiecyclops baylyi Fiers, 2001, Pescecyclops laurentiisae Karanovic, 2004, and others)or to some other parts of the world. However, the majority of the highly halotolerant species has a wide geographic distribution. One of the most widespread Palearctic species is A . salinus, whose distribution ranges from India and Algeria in the south(about 20°–21°N)(Samraoui, 2002; Boxshall, 2009)to the lower reaches of the River Ob(Russia)in the north(about 65°N)(Semenova et al., 2000), and from Spain and Morocco in the west(about 5°E)(Alonso, 1990; Rokneddine and Chentoufi, 2004)to China in the east(about 110°E)(Zhao et al., 2005). Cletocamptus retrogressus has a very similar distribution(Shen et al., 1963; Dumont and Decraemer, 1977; Alonso, 1990; Ramdani et al., 2001; Litvinenko et al., 2009; Alonso, 2010; Amarouayache et al., 2012). Apocyclops dengizicus(Lepeshkin, 1900)inhabits water bodies in Eurasia, Africa, Australia, and North America(Hammer, 1986; Tiffany et al., 2002; Pinder et al., 2005; Carrasco and Perissinotto, 2012). Diacyclops bisetosus(Rehberg, 1880)was found around the Palearctic, in North and South America, Australia, and New Zeal and (Gurney, 1933; Andrew et al., 1989; Dussart and Defaye, 2006). Cosmopolitism of the hypersaline biota was discussed previously(Por, 1980).

What peculiarities promote the wide distribution of highly halotolerant copepod species? Among such peculiarities there is high tolerance to salinity, temperature and other factors in adults. Copepods inhabiting hypersaline waters have resting stages(Moscatello and Belmonte, 2009; Anufriieva and Shadrin, 2014b)that are tolerant to digestive enzymes of birds(Radzikowski, 2013). Long-distance transportation of copepod resting stages by birds occurs(Frisch et al., 2007). Some recent invasions of alien copepod species in different regions may be explained by this way(Reid and Reed, 1994; Anufriieva et al., 2014).

Copepods are found in hypersaline waters worldwide; adults of some species can survive at salinity up to 300–360 g/L. High halotolerance in osmoconforming copepods may be explained by the consumption of exoosmolytes, mainly with food. High tolerance to many factors in adults, availability of resting stages, and an opportunity of long-distance transportation of resting stages by birds and /or winds are responsible for the wide geographic distribution of copepods inhabiting hypersaline waters. However, we know little about mechanisms that support existence of copepods in harsh hypersaline environment and their wide distribution; these deserve further in-depth study.