International Journal of Aquatic Science ISSN: 2008-8019 Vol 1, No 1, 2010

-Review- The Brine Shrimp Artemia and hypersaline environments microalgal composition: a mutual interaction

Fereidun Mohebbi Iranian Artemia Research Center, Urmia, Iran

Abstract Hypersaline environments are essential, integral and dynamic part of the biosphere. Their management and protection depend on an understanding of the influence of salinity on biological productivity and community structure. The aim of this study was to review the relationships between the two basic biological components of hypersaline environments (micro- and Artemia) to provide a better understanding the dynamics of these unique ecosystems. Algal composition as the main food source of Artemia determines Artemia growth, reproduction rates, brood size, density, lipid index and cysts yields. Furthermore, the reproduction mode of Artemia depends on food levels, so that at the low food levels the main reproduction going into cysts. On the other hand, seasonal fluctu-ations of algal abundance influence Artemia population in temperate large hypersaline lakes such as the Great Salt Lake (USA), Urmia Lake (Iran) and Mono Lake (USA). However, Artemia grazing pressure has significant effects on microalgal density.

Key Words: Artemia, hypersaline, microalgal composition,

Introduction such environments are affected by both human Hypersaline environments are important natural activities and natural dynamics. For example, assets of considerable economic, ecological, recent climatic changes have led to increasingly scientific and natural value. These ecosystems intense monsoon rains in some regions and to span large areas worldwide, not only in salt decreasing precipitation levels in others (Das production areas (solar salt works, salterns or Sarma, 2007). However, increased drought in arid Salinas) but also in natural lakes and lagoons, and and semi-arid regions of the world, which most of in tidal ponds (Javor, 1989). Hypersaline the inland hypersaline lakes are located on, had environments of both marine and continental dramatic effects on these sensitive ecosystems. In origin are essential, integral and dynamic part of fact, inland hypersaline lakes within closed the biosphere while the biogeochemical processes hydrologic basins are subjected to natural and occurring in their unique ecosystems have induced fluctuations in size and salt concentration considerable environmental, social and economic over both short and long term intervals (Herbst values (Shadrin, 2009). Interestingly, their unique and Blinn, 1998). physical and chemical characterization and Hypersaline environments are generally defined as distinctive biota set them apart from other aquatic those containing salt concentrations in excess of ecosystems (Naceur et al., 2009). Hypersaline sea water - 3.5% total dissolved salts (Das sarma environments and biodiversity associated with and Arora, 2001). Velasco et al (2006) studied the ( ) [email protected]

Mohebbi (2010) effects of salinity changes on the biotic necessary, the abiotic parameters have been communities in a Mediterranean hypersaline argued. So, the objective of the present study was stream. They suggested that the number of taxa, to attempt to provide a review based on the Margalefʼs index and Shannonʼs diversity index recent and previous studies on relationships decreased with increasing salinity. Their results between the two basic biological components in supported the initial hypothesis that dilution hypersaline environments i.e. microalgae and causes an increase in richness and biotic diversity, Artemia in order to provide a better understanding but a reduction in abundance. In other words, as the dynamics of these unique ecosystems (Jellison noted Borowitzka (1981): the more saline the and Melack, 1988). water, the lower the species diversity and simpler the structure of the system. The number of Algal composition studies that has been performed on Artemia- Both prokaryotic and eukaryotic algae grow, and phytoplankton ecological relationships in natural contribute to primary production in high salt biotopes is very limited; in most cases these concentration waters (Borowitzka, 1981). studies refer to small-sized salt lakes, or to man- made salt ponds (e.g. Herbst, 2006; Tanner et Solar saltworks al., 1999; Warnock et al., 2002). Persoone and The cyanobacterial mats of the solar lakes can be Sorgeloos (1980) and Lenz (1987) reviewed divided into two layers, the upper layer was literature data on the productivity of Artemia dominated by coccoide forms such as habitats in natural environments, both inland and Aphanothece stagnina (Sprengel) A.Braun, 1865 coastal salt lakes. and Synechococcus sp., while the lower was Management and protection of these changing dominated by filamentous species composed ecosystems depend upon an understanding of the mainly of Oscillatoria and Spirulina species influence of salinity on biological productivity and (Gamila, 1999). On the other hand, the community structure. In other words, salinity microalgae of solar saltworks may be classified changes both directly or indirectly affects the according to salinity tolerance, namely halobiont primary production which in turn may influence (salinity range 115 to 185 ppt) such as Anacystis, Artemia, as the major macrozooplankton of Dunaliella and Spirulina; halophilic (which can hypersaline waters. On the other hand, Artemia tolerate salinity range of 41 to 150 ppt) including population is able to influence phytoplankton Lyngbya, Oscillatoria, Gloeocapsa, Synura, composition by feeding on them; therefore there Amphora, Navicula spp. Nitzschia spp. and is a continuous reciprocal interaction between Surirella; stenohaline which are abundant below Artemia and phytoplankton population in 41 ppt, e.g. Chaetoceros, Gyrosigma, Amphora hypersaline environments. Although, abiotic marina W.Smith, 1857, etc (Rahaman, 2006). parameters such as temperature, salinity etc. Williams (1981) suggested that the dissolved which form a background for biological activities oxygen concentrations may well be important in and governed on these interactions, but since determining salinity tolerance in halobionts and in these ecological factors have been studied more certain halophiles. Dolapsakis et al (2005) frequently, so in this study we only focused on the concluded that in higher salinities interactions between Artemia and algae in (Dunal) Teodoresco, 1904, was able to increase hypersaline environments. However, when its ratio to more than 50% and displace other

Int. J. Aqu. Sci; 1(1):19-27, 2010 20 The Brine Shrimp Artemia and hypersaline environments… hypersaline microalgae, possibly as a better though valuable, are tougher for the Artemia to resource competitor. digest. Temperate lakes The primary producers of benthic habitat in In temperate hypersaline lakes, salinity as the hypersaline lakes are dominated by cyanobacteria major dominant parameter determines phyto- and some diatoms with the occasional green plankton species composition and diversity. In algae. The benthic primary producers are parti- most of these lakes, Dunaliella spp. mostly cularly active when the phytoplankton and brine dominate other microalgae, due to their higher shrimp density decline in the water column and salinity tolerance. For example, in the Great Salt resulting clear water allows light to penetrate to Lake it has been found that when salinity was the bottom. near 200 g/l, the phytoplankton community was Microalgal composition of Urmia Lake is roughly nearly a monoculture of Dunaliella viridis E.C.- similar to the phytoplankton in the Great Salt Teodoresco, 1905, and nitrogen fixing Lake, which consists predominantly of Dunaliella, cyanobacteria were absent or rare in the pelagic with an important fraction of diatoms like region of the lake (Rushforth and Felix, 1982), but Nitzschia and Navicula (Sorgeloos, 1997). when salinity decreased to about 50 g/l not only However, other algae such as cyanobacteria have the density of phytoplankton increased, but also contributed in microalgal composition of Urmia nitrogen fixing Nodularia sp. was detected in the Lake at more limited extent. For example, lake. (Wurtsbaugh and Berry, 1990). Stephens Mohebbi et al (2006) reported 3 cyanobacteria and Gillespie (1976) demonstrated that when the (Anabaena, Oscillatoria and Synechoccus) 2 green lake salinity was higher and nitrogen-fixing cyano- algae (Dunaliella and Ankistrodesmus) 11 diatoms bacteria absent, nitrogen deficiency may have (Navicula, Nitzschia, Cyclotella, Symbella, contributed to the summer decline in Synedra, Pinnullaria, Diatoma, Amphiprora, phytoplankton. Surirella, Cymatopleura and Gyrosigma). Reyahi Wurtsbaugh and Gliwicz (2001) suggested that et al (1994) observed 6 cyanobacteria (Anabaena, the pelagic community of phytoplankton in the Anacystis, Chrococcus, Lyngbya, Oscillatoria and Great Salt Lake during periods that Artemia were Synechoccus) 4 (Ankistrodesmus, present as juveniles or adults (from Mars to June) Dunaliella, Monostroma and pandorina) 2 diatoms was dominated by the unicellular green alga (Amphora and Navicula). These variations may be Dunaliella viridis E.C.Teodoresco, 1905, with more related to limited and irregular sampling or than 99% of the numbers of phytoplankton and increased salinity of the lake during recent years between 84 and 99% of the biovolume. The that likely has eliminated some non-tolerant densities of this alga were between 2800 and species (Eimanifar and Mohebbi, 2007). 4130 cells ml-1. Other algae such as diatoms Quantitative analysis of chlorophyll a and algal Amphiprora sp. And Amphora sp. contributed density indicated that primary production in Urmia modestly to the biovolume on some dates. In the Lake is lower than that of its sister the Great Salt Great Salt Lake two genera of cyanobacteria Lake and that Dunaliella is the dominant namely Aphanothece and Coccochloris with the phytoplankton (more than 95% of the total Dunaliella spp. along with the dozen or so phytoplankton in number) of both lakes (Van bacterial species provide the food for grazing brine Stappen et al,. 2001; Gliwicz et al., 1995 and shrimp. Due to their thick silica cell walls, diatoms Mohebbi et al., 2006).

Int. J. Aqu. Sci; 1(1):19-27, 2010 21 Mohebbi (2010)

Halotolerant algae of the genus Dunaliella are the the mouth, broken into smaller pieces or most ubiquitous eukaryotic microorganisms in discarded (Borradale and Potts, 1967). Digestion hypersaline environments which can survive even begins with the mandibles reducing the size of in saturated salt solutions. In Urmia Lake as the food particles and with the addition of a sticky second largest hypersaline lake in the world secretion from glands near the mouth. The Dunaliella was the dominant phytoplankton all secretion helps hold the bolus together while seasons (Mohebbi et al., 2009). The much more secretions all along the digestive tract add salinity near saturation (>330 ppt) induced Urmia digestive enzymes (Brown 1960). The food is Lake Dunaliella to accumulate large amounts of passed into the mouth, through esophagus and beta-carotene in their (Mohebbi et al., into the combined stomach and intestine. unpublished data). This is a mechanism by which Nutrients are taken up all along the digestive tract this alga is able to tolerate stress conditions such before the waste is passed on through the anus. as high irradiance and salinity (López-Uc et al., (Borradale and Potts, 1967). 2009; Garcia et al., 2007). It seems that algal composition as the main food More recently, a picoplanktonic (2-3µ) green alga, source of Artemia in both natural habitat and Picocystis salinarum Lewin, 2000, was described culture media has significant effect on Artemia from Mono Lake which dominates the growth and reproduction rates. For example phytoplankton community of the lake (Bruce et DʼAgostino (1980) noted that growth of Artemia al., 2008). was influenced by both the species of phytoplankton in the diet and the culture media Artemia and phytoplankton interactions used to grow the phytoplankton. According to Brine shrimp in the genus Artemia are the Wurtsbaugh and Gliwicz (2001), in the Great Salt dominant macrozooplankton present in many Lake both the quality and quantity of the food hypersaline environments (Wurtsbaugh and source, combined with temperature likely Gliwicz, 2001). This crustacean often dominates influence growth rate and time to maturation of food web dynamics in hypersaline environments Artemia, as it does in other ecothermic animals and its grazing activities control water clarity (e.g. Wurtsbaugh and Cech, 1983). Savage and (Lenz, 1987; Wurtsbaugh, 1992) and Knott (1998) studied the effects of limnological consequently they are often introduced into salt factors on parthenogenetic Artemia populations production facilities to minimize algal blooms from Lake Hayward, western Australia. They (Sorgeloos et al., 1986). The role of microalgae suggested that the major mechanism controlling and Artemia in the production of high quality salt nauplius survival and recruitment of Artemia in have been well documented (Davis, 1980). Lake Hayward was food quality and quantity. Brine shrimp are non-selective filter feeders Low spring temperatures slow growth rates of feeding on detritus scraped up from the bottom of Artemia in the Great Salt Lake (Wirick, 1972) and the water column or on unicellular algae and other Mono Lake (Dana et al., 1995). In the summer, plankton higher up in the water column. Among when perhaps lowered nutrient inputs and high other functions the rhythmic beating of the limbs grazing rates (Wurtsbaugh, 1992) decrease pumps food and water through the median gully phytoplankton abundance, Artemia growth is slow where the food is strained out by the limbs and (Dana et al., 1995). This occurs despite the fact retained in the food groove and later moved up to that potential growth rates of well-fed animals are

Int. J. Aqu. Sci; 1(1):19-27, 2010 22 The Brine Shrimp Artemia and hypersaline environments… maximal at midsummer lake temperatures of 25- (Berthelemy- Okazaki and Hedgecock, 1987), but 28 º C (Vanhaecke and Sorgeloos, 1980). Low food level appears to play a more important role. brood sizes and lipid indices have also been On the other hand, primary production as food related to the food limitation of the Artemia in the availability or food levels influences adult Artemia summer. densities in various hypersaline lakes. The lower In large temperate lakes such as the Great Salt production in the Great Salt Lake supports peak Lake, USA, Urmia Lake, Iran and Mono Lake, USA, summer adult densities of Artemia near 3 l-1; where salinity differences are small and have little whears the more productive Mono Lake has impact on the ecosystem and seasonal differences densities of 6-8 l-1 in the pelagic region (Conte et mainly imply temperature variations, generally al., 1988). Artemia has two generations per year. In fact, High salinity of Urmia Lake during recent years up Artemia population is declining by lack of to saturation levels (about 350 ppt) has recruitment, increased predation and thermal diminished Aremia population to less than 1 death (Lenz, 1987). Therefore, large temperate individual m-3 compared to 1 individual l-1 during lakes indicate explicit seasonal cycles with a high the high water levels (Mohammadi et al., 2009). predictability in which fluctuations from one year It seems that increased salinity inhibits cyst to another are limited. The spring burst of egg hatching, limits availability of nutrients especially (nauplii) production is well suited to saturate the unicellular algae and causes high mortality due to environment with juveniles that can exploit the excessive stressful condition. Additionally, cyst abundant phytoplankton food resource present clutch sizes of Mono Lake Artemia are nearly then. As phytoplankton abundance decreased, double those observed in the Great Salt Lake nauplii survival declined greatly and the (Dana et al., 1990) and cyst weights are equal to proportion of cysts produced increased or greater than those in the Great Salt Lake significantly (Wurtsbaugh and Gliwicz, 2001). In (R.Jellison, Pers.comm). the Great Salt Lake, early spring, when the Cysts yields in various hypersaline lakes and in primary producers have recovered from the different years can be influenced by primary previous yearʼs grazing pressure, is the only time production. For instance, in Mono Lake, Artemia of high food levels. Therefore, this is the time of produced 2.4 × 106 to 5.1 × 106 cysts m-2 during mass hatching from diaposing cysts and of intense different years, considerably more than the 6.5 × reproduction in Artemia (Wurtsbaugh and Gliwicz, 105 m-2 produced in the Great Salt Lake in 1995 2001). (Dana et al., 1990). This variation is likely Under low-food conditions, female Artemia have because of a higher rate of primary production in likely evolved mechanisms to produce cysts. Mono Lake (269-641 g C m-2 yr-1; Jellison and According to Gliwicz et al., (unpublished data) in Melack, 1993) than in the Great Salt Lake (145 g controlled laboratory experiments, Artemia C m-2 yr-1; Stephens and Gillespie, 1976). produced 70-90% cysts when food levels were Decreased salinity of the Great Salt Lake less than 2.5 µg chl a l-1 and 60-70% nauplii when dramatically declined the Artemia abundance due chl a levels were > 12 µgl-1. Other factors such as to the appearance of new predator taxa in temperature, salinity, photoperiod and brood zooplankton assemblage (Wurtsbaugh and Berry, number also contribute the mode of reproduction 1990). According to this study, small population of Artemia and other zooplankton were not able to

Int. J. Aqu. Sci; 1(1):19-27, 2010 23 Mohebbi (2010) clear the water column, thus chlorophyll a levels mode of reproduction switched from cyst remained high (5-44 µ g l-1 ) and secchi depths production to hatching eggs at low food levels in low (<2.2) throughout the year. the lake. On the other hand, Gliwicz et al., A single Artemia filters 240 mld-1 and therefore, at (unpublished data) suggested that the Artemia the average population density of 4 sub-adult and body weight in the Great Salt Lake was adult individuals per liter, this branchiopod is considerably smaller than that of the Farmington capable of filtering the entire lake volume once a Bay of the Great Salt Lake, where chlorophyll was day (Reeve, 1963). Thus the Dunaliella population much higher and Artemia less abundant due to density remains extremely low, and does the lower salinity. density of other green algae, diatoms and Artemia raised in laboratory in lake water without cyanobacteria that are able to reproduce fast added food withheld eggs in egg sacks (Gliwicz et enough to compensate for grazing losses. al., 1995). Female Artemia are prevented from According to Gliwicz (2003), in contrast to allocating sufficient resources to reproduction Dunaliella which is a typical euplanktonic species, below a threshold food concentration, which many other taxa are not suspended in the lake results in a long inter-brood interval as the water, but live in refuges where grazing losses are clutches of eggs are withheld in the brood sacs. At lower. These refuges are provided by the interiors the low food levels only 1 of 13 broods produced of the long tubular setae of Artemia exoskeleton, was ovoviviparious with the bulk of the which form the combs on the filtration reproduction going into cysts, and brood size were appendages. The exoskeleton is shed at each of relatively small (15.6) (mean ± 7.3 ISD) eggs the 13 or 14 molts necessary for Artemia to attain female-1 day-1; in contrast, in the high food levels maturity and large quantities float in the water. It 85% of broods were ovoviviparous and mean was found that diverse algal-cyanobacteria brood size was 53.6 (mean ± 24.8 ISD) eggs community that colonize long filtration female-1 day-1 (Gliwicz et al., unpublished data). appendages of Artemia, represented up to 20% of Most of the first cohort Artemia was already adult the available food for adult Artemia, when the by early May, but at the early June, the density of preferred free-swimming Dunaliella was at an juveniles was dropped to one tenth of the extremely low density in the entire the Great Salt expected value. Therefore, 90% of the second Lake southern arm. Artemia juveniles and nauplii generation hatching from ovoviviparous eggs had can not readily access the algae colonizing died, evidently because food levels had declined discarded exoskeleton which induces higher from 25 µg chl a l-1 to less than 1 µg chl a l-1 in survival in the older instars of Artemia than early June (Gliwicz et al., unpublished data). younger ones. This is evident from the seasonal changes in size distribution indicated by the Acknowledgements densities of discrete size classes (Gliwicz et al., I would like to appreciate Iranian Fisheries unpublished data). Research Organization (IFRO). I also appreciate As the food availability declines from June to Professor Wayne Wurtsbaugh for providing November: the individual Artemia lipid index valuable references. gradually decreased (Wurtsbaugh an Gliwicz, 2001); juvenile Artemia survival was held much References lower than that of full grown adults; Artemia

Int. J. Aqu. Sci; 1(1):19-27, 2010 24 The Brine Shrimp Artemia and hypersaline environments…

9 Berthelemy- Okazaki N.J. and Hedgecock D. Sorgeloos, P., Roels, O. and E.Jaspers (Eds). Universa (1987). Effects of environmental factors on cyst Press, Wetteren, Belgium. formation in the brine shrimp Artemia. In: Sorgeloos, 9 Dolapsakis N.P., Tafas T., Abatzopoulos Th. J., Ziller P., D.A. Bengston, W. Decleir and E. Jaspers (eds), S., and Economou- Amilli, A. (2005). Abundance and Artemia Research and its Applications. Vol.3. Ecology, growth response of microalgae at Megalon Embolon Culturing, Use in aquaculture. Universa Press, solar saltworks in northern Greece: An aquaculture Wetteren. Belgium; 167-182. prospect. Journal of Applied Phycology, 17, 39-49. 9 Borradale L.A. and Potts F.A. (1967). The 9 Eimanifar A. and Mohebbi F. (2007). Urmia Lake Invertebrata, A Manual for the use of Students. (Northwest Iran): a brief review. Saline Systems, 3:5. Cambridge Massachusetts: Cambridge University 9 Gamila H.A. (1999). Phytoplankton activities in Press,. hypersaline, anoxic conditions. I- Dynamics of 9 Borowitzka L.J. (1981). The microflora, Adaptations phytoplankton succession in the solar lakes (Taba, to life in extremely saline lakes. Hydrobiologia 81, 33- Egypt). Wat. Sci. Tech. Vol. 40, No. 7, 117- 125. 46. 9 García F., Freile-Pelegrın Y. and Robledo D. (2007). 9 Brown Jr. Frank A., (1960) .Ed. Selected Physiological characterization of Dunaliella sp. Invertebrate Types, New York, New York: John Wiley (, Volvocales) from Yucatan, Mexico. & Sons, Inc. Bioresource Technology 98, 1359–1365. 9 Bruce L.C., Jellison R., Imberger J. and Melack J. M. 9 Gliwicz Z.M., Wursbaugh W.A., and Szymanska E. (2008). Effect of benthic boundary layer transport on (unpublished data). Absence of predation eliminates the productivity of Mono Lake, California. Saline coexistence: Experience from the fish-zooplankton Systems, 4:11. interface (Fifty years after the “Homage to Santa 9 Conte F.P., Jellison R.S. and Starrett G.L. (1988). Rosalia"). Submitted in Hydrobiologia, 2010. Nearshore and pelagic abundances of Artemia Monica 9 Gliwicz Z.M., Wurtsbaugh W.A., and Ward A. (1995). in Mono Lake, California. Hydrobiologia 158, 173- 181. Brine Shrimp ecology in the Great Salt Lake, Utah. 9 DʼAgostino A. (1980). The vital requirement of June 1994-May 1995 Performance Report to the Utah Artemia: Physiology and nutrition. In Perssone, G., P. Division of Wildlife Resources, Salt Lake City, UT. Sorgeloos, O. Roels and E. Jaspers (eds), The Brine 9 Herbst D.B. (2006). Salinty controls on trophic Shrimp Artemia, 2. Physiology, Biochemistry, interactions among invertebrates and algae of solar Molecular Biology. Universa Press, Wetteren, Belgium: evaporation ponds in the Mojave desert and relation to 55- 82. shorebird foraging and Selenium risk. Wetlands, Vol. 9 Dana G. L., Jellison R. and Melack J.M. (1990). 26, No. 2, 475-485. Artemia monica cyst production and enrichment in 9 Herbst D.B. and Blinn D.W. (1998). Experimental Mono Lake, California, U.S.A. Hydrobiologia 197, 233- mesocosm studies on salinity effects on the benthic 243. algal community of a saline lake. Journal of Phycology, 9 Dana G. L., Jellison R. and Melack J. M. (1995). 34, 772-778. Effects of different natural regimes of temperature and 9 Javor B.J. (1989). Hypersaline environments. food on survival, growth and development of Artemia Microbiology and biogeochemistry. Spriger-Verlag, monica Verrill. J. Plankton Res. 17, 2117-2130. Berlin. 9 Das sarma Sh. (2007). Saline Systems highlights for 9 Jellison R. and Melack J.M. (1988). Photosynthetic 2006. Saline Systems, 3:1. activity of phytoplankton and its relation to 9 Das sarma Sh. and Arora P. (2001). Halophiles, environmental factors in hypersaline Mono Lake, Encyclopedia of life sciences/ Nature Publishing group California. Hydrobiologia, 158, 69-88. (www.els.net). 9 Jellison R. and Melack J.M. (1993). Algal 9 Davis J.S. (1980). Experiences with Artemia at solar photosynthetic activity and its response to meromixis saltworks. In: The brine shrimp Artemia. Vol.3. in hypersaline Mono Lake, California. Limnol. Ecology, Culturing, Use in Aquaculture. Persoon, G., Oceanogr. 38, 818-837.

Int. J. Aqu. Sci; 1(1):19-27, 2010 25 Mohebbi (2010)

9 Ryahi H., Soltani N. and Shokravi Sh. (1994). A 9 Lenz P.H. (1987). Ecological studies on Artemia: a study of Urmia Lake algae flora. Scientific Journal of review. In Sorgeloos, P., D.A. Bengston, W. Decleir Padjuhesh va Sazandegi, 25, 23-25. and E. Jaspers (eds), Artemia Research and its 9 Savage A., and Knott B. (1998). Artemia Applications, 3. Ecology, Culturing, Use in parthenogenetica in Lake Hayward, Western Australia. Aquaculture. Universa Press, Wetteren. Belgium. I. Interrupted recruitment into adult stages in 9 López-Uc Y.K., Sánchez-Estudillo L., Rojas-Herrera response to seasonal limnology. International of Salt R. and Narváez Zapata J.A. (2009). Physiological and Lake Research. 1, 1-12. molecular characterization of Dunaliella salina Mexican 9 Shadrin N.V. (2009). The Crimean hypersaline lakes: strains under saline stress. Avances en el estudio de la towards development of scientific basis of integrated Biotecnología, 47-51. sustainable management. Proceedings of the 9 Mohammadi H., Agh N., Sorgeloos P. (2009). A International Symposium/ Workshop on Biology and survey on salinity tolerance of Artemia urmiana and Distribution of Artemia. Urmia, Iran. parthenogenetic Artemia. Proceedings of the 9 Sorgeloos P. (1997). Resourse assessment of Urmia International Symposium/ Workshop on Biology and Lake Artemia cysts and biomass. In Urmia Lake Ditribution of Artemia. Urmia, Iran. Cooperatin Project, Item B, Edited by: Sorgeloos, P. 9 Mohebbi F., Asadpour Y., Esmaeili L. and Javan S. Laboratory of Aquaculture and Artemia reference (2006). Phytoplankton population dynamics in Urmia Center, Belgium, 1-114. Lake. 2 nd International Conference of Biology, Tarbiat 9 Sorgeloos P., lavens P., Leger P., Tackaert W.and Modarres University. Tehran, Iran. Versichele, (1986). Manual for culture and use of brine 9 Mohebbi F., Esmaeili L., Negarestan H. and Ahmadi shrimp Artemia in aquaculture. State University of R. (2009). Dynamics of phytoplankton population in Ghent. Faculty of Agriculture: 319 pp. Urmia Lake: Consequences on Artemia. Proceedings of 9 Stephens D.W. and Gillespie D.M. (1976). the International Symposium/ Workshop on Biology Phytoplankton production in the Great Salt Lake, Utah, and Distribution of Artemia. Urmia, Iran. and a laboratory study of algal response to 9 Naceur H.B., Jenhani A.B.R. and Romdhane M.S. enrichment. Limnol. Oceanogr. 21, 74-87. (2009). Ecobiological survey of the brine shrimp 9 Tanner R., Glenn E. P. and Moore D. (1999). Food Artemia salina from Sabkhet El Adhibet (south-east chain organisms in hypersaline, industrial evaporation Tunisia). Journal of the Marine Biological Association ponds. Water Environment Research 71, 494–505. of the United Kingdom, 89(6), 1109–1116. 9 Vanhaecke P. and Sorgeloos P. (1980). International 9 Persoone G. and Sorgeloos P. (1980). General study on Artemia. XIV. Growth and survival of Artemia aspects of the ecology and biogeography of Artemia. larvae of different geographical origin in a standard In: The brine shrimp Artemia. Vol.3. Ecology, culture test. Mar. Ecol. Prog. Ser. 3, 303-307. Culturing, Use in Aquaculture. Persoon, G., Sorgeloos, 9 Van Stappen G., Fayazi G., and Sorgeloos P. (2001). P., Roels, O. and E.Jaspers (Eds). Universa Press, International study on Artemia LXIII, Field study of Wetteren, Belgium, the Artemia urmiana (Günther, 1890) population in 9 Rahaman A.A. (2006). Plankton communities in Lake Urmiah, Iran. Hydrobiologia, 466, 133-143. hypersaline waters of Indian solar saltworks. 9 Velasco J., Millán A., hernández J., Guiérrez C., Proceedings of the 1th International conference on the Abellán P., Sánchez D. and Ruiz M. (2006). Response Ecological Importance of Solar Saltworks, Santorini of biotic communities to salinity changes in a Island, Greece. Mediterranean hypersaline stream. Saline Systems, 9 Rushforth S.R. and Felix E.A. (1982). Biotic 2:12. adjustments to changing salinities in the Great Salt 9 Warnock N., Page G.W., Ruhlen T.D., Nur N., Lake, Utah, USA. Microb.Ecol. 8, 157-161. Takekawa J. Y. and Hanson J.T. 2002. Management and conservation of San Francisco Bay salt ponds: effects of pond salinity, area, tide, andseason on

Int. J. Aqu. Sci; 1(1):19-27, 2010 26 The Brine Shrimp Artemia and hypersaline environments…

Pacific Flyway waterbirds. Waterbirds 25 (Special 9 Wurtsbaugh W.A., and Berry Th.S. (1990) Cascading Publication) 2,79–92. effects of decreased salinity on the phytoplankton, 9 Williams W.D. (1981) The limnology of saline lakes chemistry and physics of the Great Salt Lake (Utah). in western Victoria- a review of some recent studies. Can.J.Fish.Aqat.Sci. 47: 100-109. Hydrobiologia, 82, 232-259. 9 Wurtsbaugh W.A and Cech J. (1983) Growth and 9 Wirick C.W. (1972). The Dunaliella- Artemia activity in Gambusia Affinis fry: temperature and plankton community of the Great Salt Lake, Utah. M.S. ration effects. Trans. Am. Fish. Soc. 112: 653-660. Thesis, Dept of Biology, University of Utah: 20 pp. 9 Wurtsbaugh W.A., and Gliwicz Z.M. (2001) 9 Wurtsbaugh, W.A. (1992) Food- web modification by Limnological control of brine shrimp population an invertebrate predator in the Great Salt Lake dynamics and cyst production in the Great Salt Lake, (U.S.A). Oecologia 89: 168-175. Utah. Hydrobiologia 466: 119-132.

Int. J. Aqu. Sci; 1(1):19-27, 2010 27