CC BY
16Journal of Siberian Federal University. Biology 2018 11(4): 294-305
УДК 57.071.7(282.247.34)
Diversity of Fauna
in Crimean Hypersaline Water Bodies
Elena V. Anufriieva* and Nickolai V. Shadrin
A.O. Kovalevsky Institute of Marine Biological Research RAS 2 Nakhimov, Sevastopol, 299011, Russia
Received 25.09.2018, received in revised form 20.10.2018, accepted 10.12.2018
On the Crimean peninsula, there are more than 50 hypersaline water bodies, including the Sivash (the Sea of Azov), the largest hypersaline lagoon in the world. Based on the literature and our own long-term research data (2000-2017), a review of the fauna of the hypersaline waters in the Crimea is presented, including 298 species of animals belonging to 8 phyla, 14 classes and 27 orders. The variety ofphyla and classes within a particular range of salinity was shown to decrease significantly with an increase in salinity; 8 classes in 3 phyla can withstand salinities above 100 g/L, and only 4 classes (Branchiopoda, Hexanauplia, Ostracoda and Insecta) within 1 phylum (Arthropoda) occur at salinities above 200 g/L. The number of species found in a single sample also decreased with increasing salinity. However, in the range of50-120 g/L, the number of species was mainly determined by a different set offactors. The abundance of animals in the hypersaline waters of the Crimea can be very high: e.g., Nematoda - up to 1.4107 ind./m2, Harpacticoida - up to 3.5106 ind./m2, Ostracoda -up to 5.8105 ind./m2, and Moina salina - up to 1.3106 ind./m3. A characteristic feature of hypersaline water ecosystems is the fact that increases in salinity cause increasing amounts of benthic animals (Chironomidae, Harpacticoida, Ostracoda) to change their habitats from the bottom to the water column. At salinities above 120-150 g/L, there is almost no animal life at the bottom. Most of the species found in shallow hypersaline waters have a resting stage in their life cycle, which ensures their survival in abruptly changing environments, even those in ephemeral water bodies.
Keywords: fauna, crustaceans, hypersaline waters, Crimea.
Citation: Anufriieva E.V., Shadrin N.V. Diversity of fauna in Crimean hypersaline water bodies. J. Sib. Fed. Univ. Biol., 2018, 11(4), 294-305. DOI: 10.17516/1997-1389-0073.
© Siberian Federal University. All rights reserved
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC 4.0). Corresponding author E-mail address: lena_anufriieva@mail.ru
Фаунистическое разнообразие в гиперсоленых водоемах Крыма
Е.В. Ануфриева, Н.В. Шадрин
Институт морских биологических исследований имени А.О. Ковалевского РАН Россия, 299011, Севастополь, пр. Нахимова, 2
На Крымском полуострове расположено более 50 гиперсоленых водоемов, включая залив Азовского моря Сиваш, крупнейшую гиперсоленую лагуну мира. С использованием литературных
и собственных многолетних данных (2000-2017 гг.) нами дан обзор фауны гиперсоленых водоемов Крыма. Найдены представители 8 типов, 14 классов и 27 отрядов животных. Разнообразие типов и классов, существующих в определенном диапазоне солености, существенно уменьшается при росте солености: выше 100 г/л остаются представители
3 типов и 8 классов, выше 200 г/л - 1 типа (Arthropoda) и 4 классов (Branchiopoda, Hexanauplia, Ostracoda и Insecta). Общее количество видов, найденных в одной пробе, также убывает
с ростом солености. В диапазоне 50-120 г/л не соленость, а другие факторы в большей
степени определяют количество видов. Численность животных в гиперсоленых водоемах Крыма иногда достигает очень больших величин, например, Nematoda - до 1.4107 экз/м2, Harpacticoida - до 3.5106 экз/м2, Ostracoda - до 5.8105 экз/м2, Moina salina - до 1.3106 экз/м3. Особенностью экосистем гиперсоленых водоемов является то, что с увеличением солености все большая часть донных животных (Chironomidae, Harpacticoida, Ostracoda) переходит к жизни в водной толще. При солености выше 120-150 г/л на дне активных стадий животных практически не остается. Большинство видов, обитающих в гиперсоленых мелководных водоемах Крыма, имеют покоящиеся стадии, что обеспечивает их существование в озерах с резко флуктуирующей средой, нередко пересыхающих.
Ключевые слова: фауна, ракообразные, гиперсоленые водоемы, Крым.
Introduction
Hypersaline waters, common in arid and subarid regions, are among the planet's extreme biotopes (Wharton, 2002; Zheng, 2014). Alongside a high degree of salinity, other abiotic factors determine their extremity (Grant, 2004). Salinity affects other characteristics of the environment, thus shifting them into the extreme range (Shadrin, 2018). For example, an increase in salinity can alter the temperature regime significantly due to the decrease in heat capacity and heat conductivity of the solution.
It causes a rise in the maximum and a fall in the minimum temperatures, thus increasing the diurnal temperature range of the water. High salinity reduces oxygen solubility in the water (Nishri, Ben-Yaakov, 1990; Debelius et al., 2009) and in this way generates anoxic zones in water bodies (Shadrin, Anufriieva, 2013a; Shadrin et al., 2016).
In recent decades, more species inhabiting hypersaline waters have been discovered (Lamprey, Armah, 2008; Sultana et al., 2011; Amarouayache et al., 2012; Belmonte et al., 2012;
Carrasco, Perissinotto, 2012). At least 28 species of Copepoda (Crustacea) have been found to occur in hypersaline waters (> 100 g/L) across the world, and among them, 12 species are able to survive at extreme salinity levels (> 200 g/L) (Anufriieva, 2015a; Anufriieva, 2016). Studying life in extreme environments allows for a more accurate assessment of the limits of adaptability, the variety of adaptations and how they developed. These assessments are essential for a better understanding of the evolution of life on Earth and for predicting possible changes in ecosystems caused by climate change and anthropogenic impacts.
On the Crimean Peninsula, there are more than 50 hypersaline (> 35 g/L) water bodies, including the Sivash (the Sea of Azov), the largest hypersaline lagoon in the world (Fig. 1) (Fedchenko, 1870; Balushkina et al., 2009; Shadrin et al., 2016). Among them are hypersaline lakes of marine and continental origin. The ion ratio in marine lakes is the same as that in sea water, whereas continental reservoirs are sulphate lakes. All the lakes are shallow and polymictic and differ only in their size, the range of fluctuations in abiotic factors and their biota. Research into the biodiversity of Crimean
hypersaline waters has been ongoing since the mid-19th century (Fedchenko, 1870; Anufriieva et al., 2017). Since 1992, the diversity of their fauna has been studied systematically (Ivanova et al., 1994; Zagorodnyaya, Shadrin, 2004; Balushkina et al., 2009; Belmonte et al., 2012; Anufriieva et al., 2017; Shadrin et al., 2017); thus, hypersaline waters of this region are among the most thoroughly investigated worldwide. On the other hand, an analysis of the effects of salinity on biodiversity based on the entirety of the published data has never been performed.
This study aims to provide a review of the fauna in the hypersaline waters of the Crimea based on published data and the authors' own long-term observations (2000-2017) and to examine the influence of water salinity on the biodiversity of invertebrates and fishes.
Taxonomic diversity
Decades of research on the hypersaline lakes of the Crimea (Anufriieva et al., 2017) have revealed that the taxonomic diversity of invertebrates and fishes is fairly high (Table 1); species belonging to 8 phyla, 14 classes and 27 orders of animals have been discovered. The diversity of phyla and classes was shown
Fig. 1. Examined hypersaline water bodies in the Crimea • - lakes * - the Sivash
Taxon Max salinity, g/L Number of species Reference
1 2 3 4
Phylum Nematoda 190 4 Kolesnikova et al., 2008
Class Chromadorea 190 2 Kolesnikova et al., 2008
Order Monhysterida 190 2 Kolesnikova et al., 2008
Class Enoplea 190 2 Kolesnikova et al., 2008
Order Enoplida 190 2 Kolesnikova et al., 2008
Phylum Rotifera 190 4 Zagorodnyaya et al., 2008; Balushkina et al., 2009
Class Eurotatoria 190 4 Zagorodnyaya et al., 2008; Balushkina et al., 2009
Order Ploima 190 2 Zagorodnyaya et al., 2008; Balushkina et al., 2009
Order Flosculariaceae 100 2 Dagaeva, 1927; Balushkina et al., 2009
Phylum Platyhelminthes 100 2 Kulagin, 1888; Dagaeva, 1927
Class Turbellaria 100 2 Kulagin, 1888; Dagaeva, 1927
Order Macrostomorpha 100 1 Dagaeva, 1927
Order Proseriata 100 1 Dagaeva, 1927
Phylum Annelida 80-100 2 Shadrin et al., 2016
Class Polychaeta 80-100 2 Shadrin et al., 2016
Order Phyllodocida 80-100 2 Zagorodnyaya et al., 2008; Shadrin et al., 2016
Phylum Bryozoa 80 1 Kulagin, 1888
Class Gymnolaemata 80 1 Kulagin, 1888
Order Ctenostomata 80 1 Kulagin, 1888
Phylum Mollusca 100 3 Shadrin, 2014
Class Bivalvia 80-100 2 Shadrin, 2014
Order Mytilida 80 1 authors' unpublished data
Order Cardiida 80-100 1 Shadrin, 2014
Class Gastropoda 80 1 Kulagin, 1888; authors' unpublished data
Order Littorinimorpha 80-100 1 Kulagin, 1888; authors' unpublished data
Phylum Arthropoda 360 55 Anufriieva et al., 2017
Subphylum Crustacea 360 40 See Table 2
Class Branchiopoda 360 6 See Table 2
Order Anostraca 360 4 See Table 2
Order Cladocera 110 2 See Table 2
Class Hexanauplia 360 18 See Table 2
Subclass Copepoda 360 18 See Table 2
Order Calanoida 300 2 See Table 2
Order Cyclopoida 212 7 See Table 2
Order Harpacticoida 360 9 See Table 2
Class Ostracoda 300 5 See Table 2
Order Podocopida 300 5 See Table 2
Class Malacostraca 200 11 See Table 2
Order Amphipoda 200 4 See Table 2
Order Decapoda 85 3 See Table 2
Continuation Table 1
1 2 3 4
Order Isopoda 85 3 See Table 2
Order Mysida 120 1 See Table 2
Subphylum Hexapoda 300 15 Przhiboro, Shadrin, 2012; Shadrin et al., 2017
Class Insecta 300 15 Przhiboro, Shadrin, 2012; Shadrin et al., 2017
Order Coleoptera 200 3 authors' unpublished data
Order Diptera 300 10 Przhiboro, Shadrin, 2012
Order Hemiptera 120 2 Anufriieva, Shadrin, 2016
Phylum Chordata 100 3 Shadrin et al., 2016; Shadrin, Anufriieva, 2013a
Infraclass Teleostei 80-100 3 Shadrin et al., 2016; Shadrin, Anufriieva, 2013a
Class Actinopterygii 80-100 3 Shadrin et al., 2016; Shadrin, Anufriieva, 2013a
Order Mugiliformes 80-100 1 Shadrin, Anufriieva, 2013a
Order Atheriniformes 80-100 1 Shadrin et al., 2016
Order Perciformes 80-100 1 Shadrin et al., 2016
to drop significantly with increasing salinity; 3 phyla and 8 classes can withstand salinities above 100 g/L, and only 1 phylum (Arthropoda) and 4 classes (Branchiopoda, Hexanauplia, Ostracoda and Insecta) occur at salinities above 200 g/L. However, many of the species inhabiting hypersaline waters (Nematoda, Platyhelminthes, Rotifera, Bryozoa, etc.) have never been studied extensively.
Currently, crustaceans are the best studied group (Table 2). The number of species studied has grown significantly from 1870 (Fedchenko, 1870) to 2017, as shown in Fig. 2. Of all the species discovered within this period, 10 species (22%) were discovered from 2012-2016. It can be seen in Fig. 2 that the curve representing the number of species has not yet approached the stationary phase; therefore, the finding of more new species can be expected. Recently, based on the analysis of the dynamics of discovering new species, we concluded that 3 to 5 species of Cyclopoida may be discovered in the lakes of the Crimea (Anufriieva et al., 2014). It should be mentioned that in the well-studied hypersaline lakes of Australia, the taxonomic diversity of the
fauna is also high (Williams et al., 1990; Timms, 1993, 2002; Kokkinn, Williams, 1988; Pinder et al., 2005).
Salinity and taxonomic diversity
An increase in salinity is associated with a decrease in the biodiversity of crustaceans in water bodies (Fig. 3). As species composition varies seasonally and yearly, the relationship between the number of species and salinity was investigated in samples of water collected at the same time in 14 different hypersaline lakes in August 2012 (Fig. 4). The number of species per sample decreased with increasing salinity. Other researchers observed a similar pattern, although the exact data could be different (Williams et al., 1990; Pinder et al., 2005; Balushkina et al., 2009; Belmonte et al., 2012). Fig. 4 shows that the number of species in the samples within the 50-120 g/L salinity interval does not correlate with salinity and is significantly more diverse than in the samples from the habitats with higher salinity. The variation coefficient of the number of species in the waters within the 50150 g/L salinity interval equals 0.49, whereas
Species Max salinity, g/L Reference
1 2 3
Class Branchiopoda Order Anostraca
Artemia salina Leach, 1819 340 Shadrin et al., 2012
A. urmiana Günther, 1899 360 Shadrin, Anufriieva, 2017
Parthenogenetic populations Artemia 360 Shadrin et al., 2012
Phallocryptus spinosa (Milne-Edwards, 1840) 85 Shadrin et al., 2009
Order Cladocera
Moina salina Daday, 1888 110 Zagorodnyaya, Shadrin, 2004
Daphnia atkinsoni Baird, 1859 45 authors' unpublished data
Class Hexanauplia Subclass Copepoda Order Calanoida
Acartia tonsa Dana, 1849 55 Shadrin, Anufriieva, 2013a
Arctodiaptomus salinus (Daday, 1885) 300 Anufriieva, 2015a
Order Harpacticoida
Canuellaperplexa Scott T. et al., 1893 100 Zagorodnyaya et al., 2008
Cletocamptus retrogressus Schmankevitsch, 1875 360 Anufriieva, 2015a
Harpacticus littoralis Sars G.O., 1910 70 Kolesnikova et al., 2017
Mesochra lilljeborgii Boeck, 1865 240 Tseeb, 1958
M. rapiens (Schmelin, 1894) 240 Tseeb, 1958
M. rostrata Gurney, 1927 240 Tseeb, 1958
Metis ignea ignea Philippi, 1843 260 Anufriieva, 2015a
Microarthridion littorale (Poppe, 1881) 70 Kolesnikova et al., 2017
Nitokra spinipes spinipes Boeck, 1865 240 Tseeb, 1958
Order Cyclopoida
Acanthocyclops sp. 212 Anufriieva et al., 2014
A. americanus (Marsh, 1893) 80 Anufriieva, Shadrin, 2012
Cyclops furcifer Claus, 1857 150 Anufriieva et al., 2014
Diacyclops sp. 150 Anufriieva et al., 2014
D. bisetosus (Rehberg, 1880) 150 Anufriieva et al., 2014
Eucyclops sp. 150 Anufriieva et al., 2014
Thermocyclops crassus (Fischer, 1853) 120 authors' unpublished data
Class Ostracoda Order Podocopida
Cyprideis torosa (Jones, 1850) 70 Drapun et al., 2017
Cytherois cepa Klie, 1937 70 Drapun et al., 2017
Eucypris mareotica (Fischer, 1855) 300 Jia et al., 2015
Loxoconcha aestuarii Marinov, 1963 70 Drapun et al., 2017
L. bulgarica Caraion, 1960 70 Drapun et al., 2017
1 2 3
Class Malacostraca Order Isopoda
Idotea balthica (Pallas, 1772) 85 Shadrin, Anufriieva, 2013a
Lekanesphaera hookeri (Leach, 1814) 58 authors' unpublished data
Sphaeroma serratum (Fabricius, 1787) 85 authors' unpublished data
Order Amphipoda
Echinogammarus olivii (Milne-Edwards, 1830) 45 Anufriieva, Shadrin, 2012
Gammarus aequicauda (Martynov, 1931) 200 authors' unpublished data
Orchestia gammarellus Pallas, 1766 75 Anufriieva, Shadrin, 2012
Orchestia mediterranea Costa, 1853 75 Anufriieva, Shadrin, 2012
Order Mysida
Mesopodopsis slabberi (Van Beneden, 1861) 120 Shadrin, Anufriieva, 2013a
Order Decapoda
Carcinus maenas (Linnaeus, 1758) 85 Kulagin, 1888
Hippolyte leptocerus (Heller, 1863) 55 Shadrin, Anufriieva, 2013a
Palaemon elegans Rathke, 1837 40 authors' unpublished data
Fig. 2. The number of crustacean species found in Crimean hypersaline water bodies
2 40 1
30 -
и v ft 5Я Чн О и eu
-л
s
s
z
20 10 H
y = -16.311n(x) +102.2 R2 = 0.935
100 200 300 Salinity, g/1
400
Fig. 3. The number of crustacean species occurring at different salinities in Crimean hypersaline waters
.a lo -I
о а» Р.
î-v Л
S в
z
6
4 -2 -
0
y = 10.773е~°-00бх R2 = 0.808
0 100 200 300 400 Salinity, g/1
Fig. 4. Number of animal species per sample as a function of water salinity (August 2012)
that in the range of 200-300 g/L equals 0.28. This might be explained by the fact that many species demonstrate halotolerance within the high salinity interval and can survive in such environments. Within the lower salinity interval (from 50 to 120 g/L), different factors must determine the number of species, as was also shown in the lakes from other regions (Williams, 1998; Pinder et al., 2005). The survival of animals in hypersaline waters is permitted by two mechanisms: osmoregulation of salt concentrations in the body liquids and/or the accumulation of osmolytes inside the cells, similar to the case in single-cell organisms (Khlebovich, Aladin, 2010; Shadrin, Anufriieva, 2013b; Shadrin et al., 2017). The ability of some species to survive in hypersaline waters may depend on the concentration of algae accumulating high amounts of osmolytes in their cells (Shadrin, Anufriieva, 2013b; Anufriieva, 2015a; Shadrin et al., 2017). Among the many causes affecting biodiversity may be abiotic (oxygen concentration, temperature, etc.) as well as biotic factors (predators, competitors and the amount and quality of food) (Kokkinn, Williams, 1998; Wurtsbaugh, 1992; Shadrin et al., 2012). According to V.S. Ivlev, biotic factors are crucial for the survival of most animals, and only at critical values can abiotic factors be of the same significance (Ivlev, 1955). V.D. Williams came to a similar conclusion about the role of biotic and abiotic factors in saline lakes (Williams, 1998). Salinity is considered to be a critical factor when it reaches values above 120-150 g/L.
Animal abundance and possible applications
The animal abundance in the hypersaline lakes of the Crimea can be high (Table 3), which means that animal species play an important role in the trophic chains of these waters
(Balushkina et al., 2009). In other regions, similar observations have been made (Kokkinn, Williams, 1988; Wurtsbaugh, 1992; Lamptey, Armah, 2008; Amarouayache et al., 2012; Carrasco, Perissinotto, 2012). Arthropoda species normally constitute 70 to 100% of the abundance and biomass.
The hypersaline waters of the Crimea are common habitats for many species of birds, such as wintering, nesting and feeding grounds, during their seasonal migrations. Invertebrates are a very important constituent of bird diets, especially for Himantopus himantopus (Linnaeus, 1758), Tadorna tadorna (Linnaeus, 1758), Tringa totanus (Linneaus, 1758), Recurvirostra avosetta (Linneaus, 1758), Calidris ferruginea Pontoppidan, (1763), etc. (Khomenko, 2003; Khomenko, Shadrin, 2009).
A characteristic feature of hypersaline water ecosystems is the fact that increases in salinity cause increasing amounts of benthic animals (Chironomidae, Harpacticoida, Ostracoda) to change their habitats from the bottom to the water column (Shadrin et al., 2016; Shadrin et al., 2017). At salinities above 120-150 g/L, there is almost no animal life at the bottom. Most of the species found in shallow hypersaline waters have a resting stage in their life cycle (Moscatello, Belmonte, 2009; Shadrin et al., 2015), which ensures their survival in abruptly changing environments of water bodies that are frequently ephemeral.
Many of the abundant species, such as the rotifer Brachionus plicatilis Müller, 1786, the crustaceans Artemia spp., Moina salina, Daphnia atkinsoni, Cletocamptus retrogressus, Arctodiaptomus salinus, and Chironomidae larvae, are prospective food sources in aquaculture (Anufriieva, 2015b) because they are tolerant to high temperatures and salinity, can resist oxygen deficiency, have resting stages in their life cycles and are easy to cultivate.
Table 3. Maximum abundance of different animal taxa in the hypersaline waters of Crimea
Animal taxon Plankton, ind./m3 Floating green algae mat, ind./m2 Benthos, ind./m2 Reference
Nematoda - 1.4107 6.0105 Kolesnikova et al., 2008
Harpacticoida 7.8105 2.5-106 3.5106 Zagorodnyaya et al., 2008; Kolesnikova et al., 2008; Kolesnikova et al., 2017
Artemia spp. 5.6104 - - Zagorodnyaya et al., 2008
Moina salina 1.3-106 - - Zagorodnyaya, Shadrin, 2004; Zagorodnyaya et al., 2008
Arctodiaptomus salinus 3.1105 - - Anufriieva, Shadrin, 2015
Gammarus aequicauda - 1.8104 - Ivanova et al., 1994
Ostracoda 2.0105 5.4105 5.8105 Drapun et al., 2017
Chironomidae larvae 8.0103 3.0103 9.0103 Ivanova et al., 1994; Shadrin et al., 2017
Conclusion
In the hypersaline waters of the Crimea, similar to other regions, the fauna is diverse. The animal diversity decreases with increasing water salinity. However, in every case, there are other factors that influence the number of species. The animal abundance in the hypersaline waters of the Crimea can be high and serve as an important biological resource.
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Acknowledgements
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