Cite this paper:
Elena V. ANUFRIIEVA. Do copepods inhabit hypersaline waters worldwide? A short review and discussion[J]. Journal of Oceanology and Limnology, 2015, 33(6): 1354-1361

Do copepods inhabit hypersaline waters worldwide? A short review and discussion

Elena V. ANUFRIIEVA1,2
1 MLR Key Laboratory of Saline Lake Resources and Environments, Institute of Mineral Resources, CAGS, Beijing 100037, China;
2 Institute of Biology of the Southern Seas, Sevastopol 299011, Russia
Abstract:
A small number of copepod species have adapted to an existence in the extreme habitat of hypersaline water. 13 copepod species have been recorded in the hypersaline waters of Crimea (the largest peninsula in the Black Sea with over 50 hypersaline lakes). Summarizing our own and literature data, the author concludes that the Crimean extreme environment is not an exception: copepod species dwell in hypersaline waters worldwide. There are at least 26 copepod species around the world living at salinity above 100;among them 12 species are found at salinity higher than 200. In the Crimea Cletocamptus retrogressus is found at salinity 360×10-3 (with a density of 1 320 individuals/m3) and Arctodiaptomus salinus at salinity 300×10-3 (with a density of 343 individuals/m3). Those species are probably the most halotolerant copepod species in the world. High halotolerance of osmoconforming copepods may be explained by exoosmolyte consumption, 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 these halophilic copepods.
Key words:    Copepoda|halotolerance|exoosmolytes|biogeography   
Received: 2014-12-10   Revised: 2015-03-16
Tools
PDF ( KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Elena V. ANUFRIIEVA
References:
Aladin N V, Plotnikov I S. 2008. Modern fauna of residual water bodies formed on the place of the former Aral Sea.Proc. Zool. Inst. RAS, 312 (1-2): 145-154. (in Russian)
Alonso M. 1990. Anostraca, Cladocera and Copepoda of Spanish saline lakes. Hydrobiologia, 197 (1): 221-231, http://dx.doi.org/10.1007/BF00026952.
Alonso M. 2010. Branchiopoda and Copepoda (Crustacea) in Mongolian saline lakes. Mongolian J. Biol. Sci., 8 (1):9-16.
Amarouayache M, Derbal F, Kara M H. 2012. Note on the carcinological fauna associated with Artemia salina(Branchiopoda, Anostraca) from Sebkha Ez-Zemoul(northeast Algeria). Crustaceana, 85 (2): 129-137, http://dx.doi.org/10.1163/156854012X623728.
Andrew T E, Cabrera S, Montecino V. 1989. Diurnal changes in zooplankton respiration rates and the phytoplankton activity in two Chilean lakes. Hydrobiologia, 175 (2): 121-135, http://dx.doi.org/10.1007/BF00765123.
Anufriieva E V, Hołyńska M, Shadrin N V. 2014. Current invasions of Asian Cyclopid species (Copepoda:Cyclopidae) in Crimea, with taxonomical and zoogeographical remarks on the hypersaline and freshwater fauna. Annales Zoologici, 64 (1): 109-130, http://dx.doi.org/10.3161/000345414X680636.
Anufriieva E V, Shadrin N V. 2012. Crustacean diversity in hypersaline Chersonessus Lake (Crimea). Opt. Protect.Ecosyst., 7: 55-61. (in Russian)
Anufriieva E V, Shadrin N V. 2014a. Arctodiaptomus salinus(Daday 1885) (Calanoida, Copepoda) in saline water bodies of the Crimea. Morskoi Ecologicheskii Zhurnal, 13 (3): 5-11. (in Russian)
Anufriieva E V, Shadrin N V. 2014b. Resting stages of crustaceans in the Crimean hypersaline lakes (Ukraine)and their ecological role. Acta Geol. Sin., 88 (Suppl. 1):46-49, http://dx.doi.org/10.1111/1755-6724.12266_3.
Anufriieva E V. 2014. Free-living Cyclopidae (Copepoda, Cyclopoida) in saline and hypersaline water bodies of the Crimea: new findings. Morskoi Ecologicheskii Zhurnal, 13 (2): 24-30. (in Russian)
Balushkina E V, Golubkov S M, Golubkov M S, Litvinchuk L F, Shadrin N V. 2009. Effect of abiotic and biotic factors on the structural and functional organization of the saline lake ecosystems. Zhurnal Obshchei Biologii, 70 (6): 504-514. (in Russian)
Bayly I A E, Boxshall G A. 2009. An all-conquering ecological journey: from the sea, calanoid copepods mastered brackish, fresh, and athalassic saline waters.Hydrobiologia, 630 (1): 39-47, http://dx.doi.org/10.007/s10750-009-9797-6.
Bayly I A E. 1967. The fauna and chemical composition of some athalassic saline waters in New Zealand. New Zealand J. Mar. Freshw. Res., 1 (2): 105-117, http://dx.doi.org/10.1080/00288330.1967.9515197.
Bayly I A E. 1970. Further studies on some saline lakes of south-east Australia. Austr. J. Mar. Freshw. Res., 21 (2):117-130.
Bayly I A E. 1972. Salinity tolerance and osmotic behavior of animals in athalassic saline and marine hypersaline waters. Ann. Rev. Ecol. Syst., 3 (1): 233-268, http://www.jstor.org/stable/2096848.
Beadle L C. 1943. An ecological survey of some inland saline waters of Algeria. J. Linnean Soc. London Zool., 41 (278):218-242, http://dx.doi.org/10.1111/j.1096-3642.1943.tb01698.x.
Belmonte G, Moscatello S, Batogova E A, Pavlovskaya T, Shadrin N V, Litvinchuk L F. 2012. Fauna of hypersaline lakes of the Crimea (Ukraine). Thalassia Salentina, 34:11-24, http://dx.doi.org/10.1285/i15910725v34p11.
Ben-Amotz A, Sussman I, Avron M. 1982. Glycerol production by Dunaliella. Experientia, 38 (1): 49-52, http://dx.doi.org/10.1007/BF01944527.
Boxshall G. 2009. Freshwater Animal Diversity Assessment(FADA) Project. Crustacea-Copepoda checklist. http://fada.biodiversity.be/CheckLists/Crustacea-Copepoda.pdf.
Britton R H, Johnson A R. 1987. An ecological account of a Mediterranean salina: the Salin de Giraud, Camargue (S.France). Biol. Conserv., 42 (3): 185-230, http://dx.doi.org/10.1016/0006-3207(87)90133-9.
Brucet S, Boix D, Gascón S, Sala J, Quintana X D, Badosa A, Søndergaard M, Lauridsen T L, Jeppesen E. 2009. Species richness of crustacean zooplankton and trophic structure of brackish lagoons in contrasting climate zones: north temperate Denmark and Mediterranean Catalonia (Spain).Ecography, 32 (4): 692-702, http://dx.doi.org/10.1111/j. 1600-0587.2009.05823.x.
Burton R S. 1991. Regulation of proline synthesis during osmotic stress in the copepod Tigriopus californicus. J.Exp. Zool., 259 (2): 166-173, http://dx.doi.org/10.1002/jez.1402590204.
Carrasco N K, Perissinotto R. 2012. Development of a halotolerant community in the St. Lucia Estuary (South Africa) during a hypersaline phase. PloS One, 7 (1):e29927, http://dx.doi.org/10.1371/journal.pone.0029927.
Chen H, Jiang J G. 2009. Osmotic responses of Dunaliella to the changes of salinity. J. Cell. Physiol., 219 (2): 251-258, http://dx.doi.org/10.1002/jcp.21715.
De Miranda M A, Durante L, Serra E. 2000. Zoocenoses dans les bassins de premiére evaporation dans une saline de la Sardaigne. Mediterránea: Serie de Estudios Biológicos, Época II, 17: 45-50, http://hdl.handle.net/10045/6546.
De Vooys C G N, Geenevasen J A J. 2002. Biosynthesis and role in osmoregulation of glycine-betaine in the Mediterranean mussel Mytilus galloprovincialis LMK.Comp. Biochem. Physiol. B: Biochem. Mol. Biol., 132 (2):409-414, http://dx.doi.org/10.1016/S1096-4959(02)00052-0.
Dumont H J, Decraemer W. 1977. On the continental copepod fauna of Morocco. Hydrobiologia, 52 (2-3): 257-278, http://dx.doi.org/10.1007/BF00036451.
Dussart B H, Defaye D. 2006. World directory of Crustacea Copepoda of inland waters II-Cyclopiformes. Backhuys Publisher, Leiden. 354p.
Fenchel T. 1988. Marine plankton food chains. Ann. Rev. Ecol.Syst., 19 (1): 19-38, http://www.jstor.org/stable/2097146.
Frangoulis C, Christou E D, Hecq J H. 2004. Comparison of marine copepod outfluxes: nature, rate, fate and role in the carbon and nitrogen cycles. Adv. Mar. Biol., 47: 253-309, http://dx.doi.org/10.1016/S0065-2881(04)47004-7.
Frisch D, Green A J, Figuerola J. 2007. High dispersal capacity of a broad spectrum of aquatic invertebrates via waterbirds. Aquat. Sci., 69 (4): 568-574, http://dx.doi.org/10.1007/s00027-007-0915-0.
Geddes N C. 1976. Seasonal fauna of some ephemeral saline waters in westren Victoria with particular reference to Parartemia zietziana Sayce (Crustacea: Anostraca). Aust.J. Mar. Freshw. Res., 27 (1): 1-22, http://dx.doi.org/10. 1071/MF9760001.
Ginatullina E N, Khodjaeva G A. 2012. Zooplankton of small drainage lakes in lower part of Amudaria under increasing salinity. Scientific Information Center of ICWC, Almaty, Kazakhstan. p.173-175. (in Russian)
Goolish E M, Burton R S. 1989. Energetics of osmoregulation in an intertidal copepod: effects of anoxia and lipid reserves on the pattern of free amino accumulation. Funct.Ecol., 3 (1): 81-89, http://www.jstor.org/stable/2389678.
Grant W D. 2004. Life at low water activity. Phil. Trans. R.Soc. London B: Biol. Sci., 359 (1448): 1 249-1 267, http://dx.doi.org/10.1098/rstb.2004.1502.
Gurney R. 1933. British Freshwater Copepoda, 3. The Ray Society, London. 384p.
Hammer U T, Hurlbert S H. 1992. Is the absence of Artemia determined by the presence of predators or by lower salinity in some saline waters? In: Roberts R D, Bothwell M L eds. Aquatic Ecosystems in Semi-Arid Regions:Implications for Resource Management. Nat. Hydrol.Res. Inst. Symposium Series 7, Environment Canada, Saskatoon. p.91-102.
Hammer U T. 1986. Saline Lake Ecosystems of the World.Springer, Dordrecht. 616p.
Hammer U T. 1993. Zooplankton distribution and abundance in saline lakes of Alberta and Saskatchewan, Canada. Int.J. Salt Lake Res., 2 (2): 111-132, http://dx.doi.org/10.1007/BF02905904.
He Z H, Qin J G, Wang H Q, Wang Z Y, Xia X. 1989. Studies on the saline and hypersaline zooplanktons from Jinnan and Yinchuan regions. Acta Hydrobiol. Sin., 13 (1): 24-37.(in Chinese with English abstract)
Imhoff J F. 1986. Survival strategies of microorganisms in extreme saline environments. A dv. S pace Res., 6 (12): 299-306, http://dx.doi.org/10.1016/0273-1177(86)90098-0.
Jones D A, Price A R G, Hughs R N. 1978. Ecology of the high saline lagoons Dawhat as Sayh, Arabian Gulf, Saudi Arabia. Estuar. Coast. Mar. Sci., 6 (3): 253-262, http://dx.doi.org/10.1016/0302-3524(78)90014-2.
Khlebovich V V, Aladin N V. 2010. The salinity factor in animal life. Herald Russ. Acad. Sci., 80 (3): 299-304, http://dx.doi.org/10.1134/S1019331610030172.
Kolesnikova E A, Mazlumyan S A, Shadrin N V. 2008.Seasonal dynamics of meiobenthos fauna from a salt lake of the Crimea. In: The Firth International Conference of Environmental Micropaleontology, Microbiology and Meiobenthology (EMMM). Chennai, India. p.155-158.
Krupa E G. 2010. Zooplankton Structure of Different Ecological Type'S Waterbodies and Rivers of Kazakhstan.Dr. Sc. Thesis, Institute of Zoology, Almaty, Kazakhstan. 200p. (in Russian)
Lindley L C, Phelps R P, Davis D A, Cummins K A. 2011.Salinity acclimation and free amino acid enrichment of copepod nauplii for first-feeding of larval marine fish.Aquaculture, 318 (3-4): 402-406, http://dx.doi.org/10. 1016/j.aquaculture.2011.05.050.
Litvinenko L I, Litvinenko A I, Boiko E G. 2009. Brine shrimp Artemia in Western Siberia Lakes. Nauka, Novosibirsk. 304p. (in Russian)
Mageed A A A. 1998. Distribution and salinity ranges of zooplankton organisms at El-Fayoum depression (El-Fayoum-Egypt). Egypt. J. Aquat. Biol. Fish., 2: 51-71.
Mageed A A A. 2006. Spatio-temporal variations of zooplankton community in the hypersaline lagoon of Bardawil, North Sinai, Egypt. Egypt. J. Aquat. Res., 32 (1): 168-183, http://hdl.handle.net/1834/1456.
Marten G G, Nguyen M, Ngo G. 2000. Copepod predation on Anopheles quadrimaculatus larvae in rice fields. J. Vector Ecol., 25 (1): 1-6.
Monchenko V I. 2003. Free-Living Cyclopoid Copepods of Ponto-Caspian Basin. Naukova Dumka, Kyiv. 350p. (in Russian)
Moore J E. 1952. The Entomostraca of southern Saskatchewan.Canad. J. Zool., 30 (6): 410-450, http://dx.doi.org/10.1139/z52-036.
Moscatello S, Belmonte G. 2009. Egg banks in hypersaline lakes of the South-East Europe. Sal. Syst., 5 (1): 3, http://dx.doi.org/10.1186/1746-1448-5-3.
Oren A. 2011. Thermodynamic limits to microbial life at high salt concentrations. Environ. Microbiol., 13 (8): 1 908-1 923, http://dx.doi.org/10.1111/j.1462-2920.2010.02365.x.
Patrick M L, Bradley T J. 2000. Regulation of compatible solute accumulation in larvae of the mosquito Culex tarsalis: osmolarity versus salinity. J. Exp. Biol., 203:831-839.
Pierce S K, Edwards S C, Mazzocchi P H, Klingler L J, Warren M K. 1984. Proline betaine: a unique osmolyte in an extremely euryhaline osmoconformer. Biol. Bull., 167 (2):495-500.
Pinder A M, Halse S A, McRae J M, Shiel R J. 2005. Occurrence of aquatic invertebrates of the wheatbelt region of Western Australia in relation to salinity. Hydrobiologia, 543 (1):1-24, http://dx.doi.org/10.1007/s10750-004-5712-3.
Por F D. 1980. A classification of hypersaline waters, based on trophic criteria. Mar. Ecol., 1 (2): 121-131, http://dx.doi.org/10.1111/j.1439-0485.1980.tb00214.x.
Radzikowski J. 2013. Resistance of dormant stages of planktonic invertebrates to adverse environmental conditions. J. Plankton Res., 35 (4): 707-723, http://dx.doi.org/10.1093/plankt/fbt032.
Ramdani M, Elkhiati N, Flower R J, Birks H H, Kraïem M M, Fathi A A, Patrick S T. 2001. Open water zooplankton communities in North African wetland lakes: the CASSARINA project. Aquat. Ecol., 35 (3-4): 319-333, http://dx.doi.org/10.1023/A:1011926310469.
Reid J W, Reed E B. 1994. First records of two Neotropical species of Mesocyclops (Copepoda) from Yukon Territory:Cases of passive dispersal? Arctic, 47 (1): 80-87, http://www.jstor.org/stable/40511533.
Rokneddine A, ChentoufiM. 2004. Study of salinity and temperature tolerance limits regarding four crustacean species in a temporary salt water swamp (Lake Zima, Morocco). Animal Biol., 54 (3): 237-253, http://dx.doi.org/10.1163/1570756042484719.
Samraoui B. 2002. Branchiopoda (Ctenopoda and Anomopoda)and Copepoda from eastern Numidia, Algeria.Hydrobiologia, 470 (1-3): 173-179, http://dx.doi.org/10. 1023/A:1015640525662.
Seibel B A, Walsh P J. 2002. Trimethylamine oxide accumulation in marine animals: relationship to acylglycerol storage. J. Exp. Biol., 205 (3): 297-306.
Semenova L A, Aleksyuk V A, Dergach S M, Leleko T I. 2000.Species diversity of zooplankton in the water bodies of the Ob North. Vestnik ekolgii, Lesovedenia I Landshavtoveniya, 1: 127-134. (in Russian)
Senicheva M I, Gubelit Y, Prazukin A V, Shadrin N V. 2008.Phytoplankton of the Crimean hypersaline lakes. In:Tokarev Yu N, Finenko Z Z, Shadrin N V eds. The Black Sea Microalgae: Problems of Biodiversity Preservation and Biotechnological Usage. ECOSI- Gidrofizika, Sevastopol. p.5-18. (in Russian)
Senicheva M I. 2005. Green alga Dunaliella salina in the natural conditions. Ecologiya Morya, 67: 61-63. (in Russian)
Shadrin N V, Anufriieva E V. 2013. Dependence of Arctodiaptomus salinus (Calanoida, Copepoda)halotolerance on exoosmolytes: new data and a hypothesis.J. Medit. Ecol., 12: 21-26.
Shadrin N V. 2009. The Crimean hypersaline lakes: towards development of scientific basis of integrated sustainable management. Wuhan, China. http://wldb.ilec.or.jp/data/ilec/WLC13_Papers/S12/s12-1.pdf.
Shadrin N V. 2012. Crustaceans in Hypersaline water bodies:the specificity of the existence and adaptation. In:Korovchinsky N M, Zhdanova S M, Krylov A V eds.Actual Problems of Crustacean Study in Continental Waters. OOO Kostroma Printing House, Kostroma.p.316-319. (in Russian)
Shen J R, Chen Y, Song D X. 1963. Notes on the Copepoda fauna of Chinghai province, China. Acta Zool. Sin., 15 (2):263-272. (in Chinese with English abstract)
Stuge T S, Matmuratov C A, Krupa E G, Akberdina G Z. 2003.Peculiarities of the plankton shrimps development in waterbodies of Semipalatinsk test range zone in 2002.Vestnik Natsional'nogo Yadernogo Tsentra Respubliki Kazakhstan, 3: 141-149. (in Russian)
Svetlichny L, Hubareva E, Khanaychenko A. 2012. Calanipeda aquaedulcis and Arctodiaptomus salinus are exceptionally euryhaline osmoconformers: evidence from mortality, oxygen consumption, and mass density patterns. Mar.Ecol. Progr. Ser., 470: 15-29, http://dx.doi.org/10.3354/meps09907.
Tiffany M A, Swan B K, Watts J M, Hurlbert S H. 2002.Metazooplankton dynamics in the Salton Sea, California, 1997-1999. Hydrobiologia, 473 (1-3): 103-120, http://dx.doi.org/10.1023/A:1016529617757.
Timms B V. 1987. Limnology of Lake Buchanan, a tropical saline lake and associated pools, of North Queensland.Austr. J. Mar. Freshw. Res., 38 (6): 877-884, http://dx.doi.org/10.1071/MF9870877.
Timms B V. 1993. Saline lakes of the Paroo, inland New South Wales, Australia. Hydrobiologia, 267 (1-3): 269-289, http://dx.doi.org/10.1007%2FBF00018808.
Timms B V. 2001. A study of the Werewilka Inlet of the saline Lake Wyara, Australia-a harbour of biodiversity for a sea of simplicity. Hydrobiologia, 466 (1-3): 245-254, http://dx.doi.org/10.1023/A:1014597131801.
Timms B V. 2009. Study of the saline lakes of the Esperance Hinterland, Western Australia, with special reference to the roles of acidity and episodicity. Nat. Res. Environ.Res. Environ. Iss., 15 (1): 215-225, http://digitalcommons.usu.edu/nrei/vol15/iss1/44.
Tseeb Y Y. 1958. Composition and quantitative development of microbenthal fauna in the downstream of the Dnieper and in the bodies of water of the Crimea. Zoologicheskii Zhurnal, 371: 3-12. (in Russian)
Van Der Meeren T, Olsen R E, Hamre K, Fyhn H J. 2008.Biochemical composition of copepods for evaluation of feed quality in production of juvenile marine fish.Aquaculture, 274 (2-4): 375-397, http://dx.doi.org/10. 1016/j.aquaculture.2007.11.041.
Vesnina L V. 2003. Structure and Functioning of Zooplankton Communities of Lake Ecosystems in South Part of West Siberia. Dr. Sc. Thesis, Altai University, Barnaul, Russia. 210p. (in Russian)
Walter T C, Boxshall G. 2015. World of Copepods. http://www.marinespecies.org/copepoda/aphia.php?p=taxdetails& id=349512. Accessed on 2015-06-17.
Williams W D, Kokkinn M J. 1988. The biogeographical affinities of the fauna in episodically filled salt lakes: a study of Lake Eyre South, Australia. Hydrobiologia, 158 (1): 227-236, http://dx.doi.org/10.1007/BF00026280.
Yancey P H. 2001. Water stress, osmolytes and proteins. Am.Zool., 41 (4): 699-709, http://dx.doi.org/10.1093/icb/41. 4.699.
Yermolayeva N I. 2012. Seasonal changes in Cladocera community in lakes of different salinity in Barabinsk-Kulunda lake province (South of Western Siberia). In:Korovchinsky N M, Zhdanova S M, Krylov A V eds.Actual Problems of Crustacean Study in Continental Waters. OOO Kostroma Printing House, Kostroma.p.187-189. (in Russian)
Zagorodnyaya Y A, Batogova E A, Shadrin N V. 2008. Longterm transformation of zooplankton in the hypersaline lake Bakalskoe (Crimea) under salinity fl uctuations.Morskoi Ecologicheskii Zhurnal, 7: 41-50. (in Russian)
Zavarzin G A. 2003. Lectures on Natural Historical Microbiology. Nauka, Moscow. 348p. (in Russian)
Zernov S A. 1949. General Hydrobiology. Akad. Nauk USSR, Moscow. 587p. (in Russian)
Zhao W, He Z H. 1999. Biological and ecological features of inland saline waters in North Hebei, China. Int. J. Salt Lake Res., 8 (3): 267-285, http://dx.doi.org/10.1023/A:1009091216842.
Zhao W, Zheng M P, Xu X Z, Liu X F, Guo G L, He Z H. 2005.Biological and ecological features of saline lakes in northern Tibet, China. Hydrobiologia, 541 (1): 189-203, http://dx.doi.org/10.1007/s10750-004-5707-0.
Copyright © Haiyang Xuebao