Biochemical Content (fatty acids, sterols, total protein, lipophilic vitamins) and Antioxidant activity (GSH, MDA) of Cladocerans (Daphnia sp., Diaphasoma branchyrum)

Year 2020, Volume: 3 Issue: 1, 34 - 46, 31.01.2020

Fatma Caf , Nurgül Şen Özdemir , Zehra Gökçe

Abstract

This paper presents biochemical content such as fatty acids, sterols, total protein, lipophilic vitamins, and antioxidant parameters of mixed cladoceran samples (Daphnia sp., Diaphanosoma brachyurum) in the freshwater ecosystem. Results indicated that predominant fatty acids were 20:5n3 (19.85%), 16:1n7 (17.29%), 16:0 (13.1%), 24:0 (12.55%), 18:0 (10.68%) and 18:1n9 (7.99%). Cholesterol was the principal sterol (194.1 µg/g) in cladocerans. Total protein was calculated as 52.26 µg/g in cladocerans. α-tocopherol (vitamin E) was the most important vitamin (4.6 µg/g) among lipophilic vitamins. Glutathione (GSH) was quite high (450µg/g) than MDA (11.5 nmol/g). 

Keywords

EPA, cholesterol, α-tocopherol, GSH

Biochemical Content (fatty acids, sterols, total protein, lipophilic vitamins) and Antioxidant activity (GSH, MDA) of Cladocerans (Daphnia sp., Diaphasoma branchyrum)

Abstract

This paper presents
biochemical content such as fatty acids, sterols, total protein, lipophilic
vitamins, and antioxidant parameters of mixed cladoceran samples (Daphnia sp., Diaphasoma branchyrum) in the freshwater ecosystem. Results
indicated that predominent fatty acids were 20:5n3 (19.85%), 16:1n7 (17.29%),
16:0 (13.1%), 24:0 (12.55%),  18:0
(10.68%) and 18:1n9 (7.99%). Cholesterol was the principal sterol (194.1 µg/g)
in cladocerans. Total protein was calculated as 52.26 µg/g in cladocerans.
α-tocopherol (vitamin E) was the most important vitamin (4.6 µg/g) among
lipophilic vitamins. Glutathione (GSH) was quite high (450µg/g) than MDA (11.5
nmol/g). 

Keywords

EPA, cholesterol, α-tocopherol

References

• Ahlgren, G., Lundstedt, L., Brett M., Forsberg C. (1990) Lipid composition and food quality of some freshwater phytoplankton for cladoceran zooplankton. Journal of Plankton Research 12: 809-818. doi: 10.1093/plankt/12.4.809.
• Aitken, R.J., Clarkson, J.S., Fishe L.S. (1989) Generation of reactive oxygen species lipid peroxidation and human sperm function. Biology of Reproduction 41: 83-197. doi: 10.1095/biolreprod41.1.183.
• Altındag, A., Buyurgan O., Kaya, M., Ozdemir, E., Dirican S. (2009) A survey on some physico-chemical parameters and zooplankton structure in Karaman Stream, Antalya. Journal of Animal and Veterinary Advances 8: 1710-1716.
• Anderson, M.E. (1998) Glutathione, an overview of biosynthesis and modulation. Chemico-Biological Interactions 111-112: 1-14. doi: 10.1016/S0009-279797)00146-4.
• Armstrong, D., Browne, R. (1994) The Analysis of Free Radicals. Lipid Peroxides. Antioxidant Enzymes And Compounds Related to Oxidative Stress as Applied to The Clinical Chemistry Laboratory, in: Armstrong, D. (Ed.), Free Radicals in Diagnostic Medicine, Advances in Experimental Medicine and Biology, I Plenum Press Vol. 366, pp. 43–58 doi: 10.1007/978-1-4615-1833-4_4.
• Arts, M.T., Ackman, R.G., Holub, B.J. (2001) “Essential fatty acids” in aquatic ecosystems, a crucial link between diet and human health and evolution. Canadian Journal of Fisheries and Aquatic Sciences 58: 122-137. doi: 10.1139/f00-224
• Ballantyne, A.P., Brett, M.P., Schindler, D.E. (2003) The importance of dietary phosphorus and highly unsaturated fatty acids for sockeye Oncorhynchus nerka growth in lake Washington–a bioenergetic approach. Canadian Journal of Fisheries and Aquatic Sciences 60: 12-22. doi: 10.1139/f02-166.
• Bandyopadhyay, D. Chattopadhyay, A. (2006) Reactive oxygen species-induced gastric ulceration, protection by melatonin. Current Medical Chemistry 13: 1187-1202. doi: 10.2174/092986706776360842.Barata, C., Varo, I., Navarro, J.C., Arun, S., Porte, C. (2005) Antioxidant enzyme activities and lipid peroxidation in freshwater cladoceran Daphinia magma exposed to redox cycling compounds. Comparative Biochemistry and Physiology Part C 140: 175-186.
• Botsoglou, N.A., Fletouris, D.J., Papageorgiou, G.E., Vassilopoulos, V.N., Mantis, A.J., Trakatellis, A.G. (1994) A rapid sensitive and specific thiobarbituric acid method for measuring lipid peroxidation in animal tissues food and feedstuff samples. Journal and Agricultural and Food Chemistry 42: 1931-1937. doi: 10.1021/jf00045a019.
• Bourdier, G., Amblard, C.A. (1989) Lipids in Acanthodiaptomus denticornis during starvation and fed on three different algae. Journal of Plankton Research 11: 1201–1212. doi,10.1093/plankt/11.6.1201.
• Brett, M.T., Muller-Navarra. D.C., Persson J. (2009) Lipids in Aquatic Ecosystems, in: Arts, M.T., Kainz M., Brett M.T. (Eds.), Crustacean zooplankton fatty acid composition, New York, Springer, pp. 115-146.
• Bulut, I. (2012) Floating Islands of Turkey. Frst. Press University of Ataturk Erzurum 181p. (in Turkish).
• Burns, C.W., Brett, M.T., Schallenberg, M.A. (2011) Comparison of the trophic transfer of fatty acids in freshwater plankton by cladocerans and calanoid copepods. Freshwater Biology 56: 889-903. doi:10.1111/j.1365-2427.
• Bychek, E.A., Gushchina, I.A. (1999) Age-dependent changes of lipid composition in Daphnia magna. Biochemistry Moscow, 64: 543-545.
• Catala, A. (2012) Lipid Peroxidation End-Products as a Key of Oxidative Stress, Effect of Antioxidant on Their Production and Transfer of Free Radicals. in: Hassan, H.A., El-Aal, M.A. (Eds.), Lipid Peroxidaxion, pp. 63-88. doi:10.5772/2929.
• Chari, T.J., Mahender, J., Kumar, A.S.M., Rajashekhar, A.V. (2013) Zooplankton Diversity Abundance and Seasonal Variation of Nagulakunta Water Tank Vinjapally Karimnagar Dist Telangana State India. International Journal of Science and Research IJSR 4(7): 1651-1654. ISSN (Online), 2319-7064.
• Christie, W.W. (1990) Gas chromatography and lipids, A practical guide. Bridgewater. Somerset, The Oily Press, England, 96p.
• Copeman, L.A., Parrish, C.C., Brown, J.A., Harel, M. (2002) Effects of docosahexaenoic eicosapentaenoic and arachidonic acids on the early growth survival lipid composition and pigmentation of yellowtail flounder Limanda ferruginea, a live food enrichment experiment. Aquaculture 210: 285-304. doi: 10.1016/S0044-84860100849-3.
• Correia, A.D., Lima, G., Costa, M.H., Livingstone, D.R. (2002) Biomarkers of copper exposure and toxicity in a marine amphipod Gammarus locusta Crustacea, Induction of metallothionein and lipid peroxidation. Biomarkers 7: 422-437. doi: 10.1080/135475002760413516
• Dalle-Donne, I., Rossi, R., Giustarini, D., Colombo, R., Milzani, A. (2007) S-glutathionylation in protein redox regulation. Free Radical Biology and Medicine 43: 883-898. doi: 10.1016/j.freeradbiomed.2007.06.014.
• Desvilettes, C.G., Boundier, G., Breton, J.C. (1997) On the occurrence of a possible bioconversion of linolenic acid into docosahexaenoic acid by the copepod Eucyclops serrulatus fed on microalgae. Journal of Plankton Research 19: 273-278. doi: 10.1093/plankt/19.2.273
• Di Giulio, R.T., Benson, W.H., Sanders, B.M., Van Veld, P.A. (1995) Biochemical mechanisms, metabolism adaptation and toxicity. in: Ran, G., (Ed.) Fundamentals of Aquatic Toxicology Effects Environmental Fate and Risk Assessment, Taylor and Francis, London, pp. 523-561.
• Dianzani, M., Barrera, G. (2008) Pathology and physiology of lipid peroxidation and its carbonyl products, in: Álvarez, S., Evelson, P. (Eds), Free Radical Pathophysiology Transworld Research Network, Kerala, India, pp. 19-38, ISBN 978-81-7895-311-3
• Doğan Demir, A., Şahin, U., Meral, R., Demir Y. (2013) Present Status of Bingöl Floating Island Wetlands and Improvement Opportunities. 3. Congress of National Wetlands. 23-25 October 2013, Book of Reports, Samsun,Turkey, pp. 85-89 (in Turkish).
• Downer, R.G.H., Kallapur, V.L. (1981) Temperature-induced changes in lipid composition and transition temperature of flight muscle mitochondria of Schistocerca gregaria. Journal of Thermal Biology 64: 189-194. doi:10.1016/0306-45658190005-X.
• Ellman, G.L. (1959) Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics 82: 70-77. doi:10.1016/0003-98615990090-6.Esterbauer, H., Cheeseman, K.H. (1990) Determination of aldehydic lipid peroxidation products, malonaldehyde and 4- hydroxynonenal. Methods in Enzymology 186: 407-421. doi,10.1016/0076-68799086134-H.
• Fidan, A.F., Ciğerci, I.H., Konuk, M., Küçükyurt, I., Aslan, R., Dündar Y. (2008) Determination of some heavy metal levels and oxidative status in Carassius carassius L. 1758 from Eber Lake. Environmental Monitoring and Assessment 1471: 35-41. doi: 10.1007/s10661-007-0095-3.
• Forró, L., Korovchinsky, N.M., Kotov, A.A., Ptrusek, A. (2008) Global diversity of cladocerans Cladocera Crustacea in freshwater. Hydrobiologia 595: 177-184. doi: 10.1007/s10750-007-9013-5.
• Funk, C.D. (2001) Prosgladins and leukotrienes, advences in eicosanoids biology. Science, 294: 1871-1875. doi:10.1126/science.294.5548.1871.
• Gama-Flores, J.L., Huidobro-Salas, M.E., Sarma, S.S.S., Nandini, S., Zepeda-Meja, R., Gulati, R.D. (2015) Temperature and age affect the life history characteristics and fatty acid profiles of Moina macrocopa Cladocera. Journal of Thermal Biology 53: 135-142. doi,10.1016/j.jtherbio.2015.10.005.
• Garg, M.L., Wood, L.G., Singh, H., Moughan, P.J. (2006) Means of delivering recommended levels of long chain n3 polyunsaturated fatty acids in human diets. Journal of Food Science 71: R66–R71. doi,10.1111/j.1750-3841.2006.00033.x.
• Gawel, S., Wardas, M., Niedworok, E., Wardas, P. (2004) Malondialdehyde MDA as a lipid peroxidation marker. Wiadomosci lekarskie 579 (10): 453-455.
• Gil, P., Farinas, F., Casado, A., López-Fernandez, M.E. (2002) Malondialdehyde, a possible marker of ageing. Gerontology, 484: 209-214. doi: 10.1159/000058352.
• Gladyshev, M.I., Sushchik, N.N., Kalachova, G.S., Dubovskaya, O.P., Makhutova, O.N. (2006) Influence of sestonic elemental and essential fatty acid contents in a eutrophic reservoir in Siberia on population growth of Daphnia longispina group. Journal of Plankton Research 28: 907-917. doi:10.1093/plankt/fbl028.
• Gladyshev, M.I., Sushchik, N.N., Dubovskaya, O.P., Makhutova, O.N., Kalachova, G.S. (2008) Growth rate of Daphnia feeding on seston in a Siberian reservoir, the role of essential fatty acid. Aquatic Ecology 42: 617-627. doi:10.1007/s10452-007-9146-7.
• Gladyshev, M.I., Arts, M.T., Sushchik, N.N. (2009) Lipids in Aquatic Ecosystems, in: Arts, M.T., Kainz, M., Brett, M.T. (Eds.), Prelimi nary estimates of the export of omega3 highly unsatur ated fatty acids EPA+DHA from aquatic to terrestrial ecosystems, Springer New York, pp. 179-209. doi: 10.1007/978-0-387-89366-2_8.
• Gladyshev, M.I., Semenchenko, V.P., Dubovskaya, O.P., Fefılova, E.B., Makhutova, O.N., Dubovskaya, O.P., Sushchik, N.N., Razlutskij, V.I., Lepskaya, E.V., Baturina, M.A., Kalachova, G.S., Kononova, O.N. (2011) Effect of temperature on contents of essential highly unsaturated fatty acids in freshwater zooplankton. Limnologica 41: 339-347. doi: 10.1016/j.limno.2011.03.001.
• Gladyshev, M.I., Sushchik, N.N., Dubovskaya, O.P., Dubovskaya, O.P., Olesia, N., Makhutova, O.N., Fefılova, E.B., Feniova, I.Y., Semenchenko, V.P., Kolmakova, A.A., Kalachova, G.S. (2015) Fatty acids composition of Cladoceraa and Copepoda from lakes of contrasting temperature. Freshwater Biology 60: 373-386. doi: 10.1111/fwb.12499.
• Goulden, C.E., Place, A.R. (1990) Fatty acid synthesis and accumulation rates in daphnids. Journal of Experimental Zoology, 256: 168-178. doi:10.1002/jez.1402560207.
• Gurr, M.I., Harvood, J.L. (1991) Lipid Biochemistry, An Introduction. Chapman and Hall, London, pp. 186-187. doi: 10.1007/978-1-4615-3862-2_1.
• Hamre, K., Lie, O. (1995) Alpha-tocopherol levels in different organs of Atlantic salmon Salmo salar L. - effect of smoltification dietary levels of n-3 polyunsaturated fatty acids and vitamin E. Comperative Biochemistry and Physiology 111A: 547-554.
• Hamre, K., Berge, R.K., Lie, O. (1998) Turnover of a-g-and y-tocopherol and distribution in subcellular and lipoprotein fractions indicate presence of a hepatic tocopherol binding protein in Atlantic salmon Salmo salar L.. Fish Physiology and Biochemistry 18: 71-83. doi: 10.1023/A,1007798102002.
• Hara, A., Radin N.S. (1978) Lipid extraction of tissues with a low-toxicity solvent. Analytica Biochemistry 901: 420-426. doi: 10.1016/0003-26977890046-5.Hartwich, M., Martin-Creuzburg, D., Wacker, A. (2013) Seasonal changes in the accumulation of polyunsaturated fatty acids in zooplankton.
• Journal of Plankton Research 351: 121-134. doi: 10.1093/plankt/fbs078.
• Harwood, J.L. (1996) Recent advances in the biosynthesis of plant fatty acids. Biochimica et Biophysica Acta 1301: 7-56. doi:10.1016/0005-27609500242-1.
• Hassett, R.P. (2004) Supplementation of a diatom diet with cholesterol can enhance copepod egg-production rates. Limnology and Oceanography 49: 488-494. doi: 10.4319/lo.2004.49.2.0488.
• Hessen, D.O. (1990) Carbon nitrogen and phosphorus status in Daphinia at varying food conditions. Journal of Plankton Research 12: 1239-1249. doi: 10.1093/plankt/12.6.1239.
• Hessen, D.O., Leu E. (2006) Trophic transfer and trophic modification of fatty acids in high Arctic lakes. Freshwater Biology 51: 1987-1998. doi: 10.1111/j.1365-2427.2006.01619.x
• Jain, S.K., Mcvie, R., Duett, J., Herbst, J.J. (1989). Erythrocyte membrane lipid peroxidation and glycosylated hemoglobin in diabetes. Diabetes 38: 1539-1542. doi: 10.2337/diab.38.12.1539.
• Kahn-Thomas, M., Enesco, H.E. (1982) Effect of α-tocopherol and culture method on reproduction of Turbatrix aceti. Journal of Nematology 14(4): 496-500.
• Kainz, M., Perga, M.E., Arts, M.T., Mazumder, A. (2009) Essential fatty acid concentrations of different seston sizes and zooplankton, a field study of monomictic coastal lakes. Journal of Plankton Research 31: 635-645. doi: 10.1093/plankt/fbp015.
• Katsanidis, E., Addis, P.B. (1999) Novel HPLC analysis of tocopherols and cholesterol in tissue. Free Radic Biology and Medicine 27: 1137-1140. doi: 10.1016/S0891-5849 9900205-1.
• Kaya, M., Fontaneto, D., Segers, H., Altındağ A. (2010) Temperature and salinity as interacting drivers of species richness of planktonic rotifers in Turkish continental waters. Journal of Limnology 69: 297-304. doi: 10.4081/jlimnol.2010.297.
• Kostner, G.M., Ottl, K., Jauhiainen, M., Ehnholm, C., Esterbaver, H. (1995) Human plasma phospho-lipids transfer protein accelerates exchange transfer of α-tocopherol between lipoproteins and cells. Biochemical Journal 305: 659-667. doi: 10.1042/bj3050659.
• Koussoroplis, A.M., Kainz, M.J., Striebel, M. (2012) Fatty acid retention under temporally heterogeneous dietary intake in a cladoceran. Oikos 122: 1017–1026. doi: 10.1111/j.1600-0706.2012.20759.x
• Lands, W.E.M. (2009) Lipids in Aquatic Ecosystems, in: Arts, M.T., Kainz, M., Brett, M.T. (Eds), Human life, caught in the food web, Springer New York, pp. 327-354. doi: 10.1007/978-0-387-89366-2_14.
• Lowry, O.H., Rosebrough, N.J., Farr, N.J., Randall R.J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biology and Chemistry 93: 265-275.
• Makhutova, O.N., Gladyshev, M.I., Sushchik, N.N., Dubovskaya, O.P., Buseva, Z.F., Fefilova, E.B., Semenchenko, V.P., Kalachova, G.S., Kononova, O.N., Baturina, M.A. (2014) Comparison of fatty acid composition of cladocerans and copepods from lakes of different climatic zones. Contemporary Problems of Ecology 7(4): 474–483. ISSN 19954255.
• Manca, M., Spagnuolo, T., Comoli P. (1994) Variations in carbon and nitrogen content with body lenght of Daphinia hyalina-galeata from laboratory and field observations. Journal of Plankton Research 16: 1303-1314. doi: 10.1093/plankt/16.10.1303.
• Mansour, M.P., Frampton, D.M.F., Nichols, P.D., Volkman, J.K., Blackburn, S.I. (2005) Lipid and fatty acid yield of nine stationary phase microalgae, applications and unusual C24–C28 polyunsaturated fatty acids. Journal of Applied Phycology 17: 287-300. doi: 10.1007/s10811-005-6625-x.
• Marnet, L.J. (1999) Lipidperoxidation-DNA damage by Malondialdehyde. Mutation Research 424: 83-95. doi:10.1016/S0027-51079900010-X.
• Martin-Creuzburg, D., Von Elert, E. 2004. Impact of 10 dietary sterols on growth and reproduction of Daphnia galeata. Journal of Chemical Ecology 303: 483-500. doi: 10.1023/B,JOEC.0000018624.94689.95.
• Martin-Creuzburg, D., Wacker, A., Von Elert, E. (2005) Life history consequences of sterol availability in the aquatic keystone species Daphnia. Oecologia 144: 362-372. doi: 10.1007/s00442-005-0090-8.
• Martin-Creuzburg, D., Wacker, A., Ziese, C., Kainz, M.J. (2012) Dietary lipid quality affects temperature-mediated reaction norms of a freshwater key herbivore. Oecologia 168: 901–912. doi: 10.1007/s00442-011-2155-1
• Masclaux, H., Bec, A., Kainz, M.J., Perriere, F., Desvilettes, C., Bourdier, G. (2012) Accumulation of polyunsaturated fatty acids by cladocerans, effects of taxonomy temperature and food. Freshwater Biology 57: 696–703.
• Meister, A., Larsson, A. (1995) Glutathione synthetase deficiency and other disorders of the gamma-glutamyl cycle. in: Scriver, C.R., Kinzler K.W., Valle, D., et al., (Eds.), The Metabolic and molecular bases of inherited diseases, New York, Mc Graw- Hill, pp. 1461-1477.
• Mourente, G., Dı́az-Salvago E. (1999) Characterization of antioxidant systems oxidation status and lipids in brain of wild-caught size-class distributed Aristeus antennatus Risso 1816 Crustacea Decapoda. Comparative Biochemistry and Physiology 1244: 405-416. doi:10.1016/S0305-04919900133-9.
• Muller-Navarra, D.C. (1995a) Evidence that a highly unsaturated fatty acid limits Daphnia growth in nature. Archiv für Hydrobiologie 132: 297-307.
• Muller-Navarra, D.C. (1995b) Biochemical versus mineral limitation in Daphnia. Limnology and Oceanography 40: 1209-1214. doi: 10.4319/lo.1995.40.7.1209.
• Muller-Navarra, D.C., Brett, M.T., Liston, A.M., Goldman, C.R. (2000) A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403: 74-77. doi: 10.1038/47469.
• Naito, Y., Yoshikawa T. (2006) Oxidative stress involvement and gene expression in indomethacin-induced gastropathy. Redox Report 11: 243-253. doi: 10.1179/135100006X155021.
• Nes WR., Mckean ML. (1977) Biochemistry of Steroids and Other Isopentenoids, University Park Press, in: Baltimore, M.D. (Eds.), University Park Press, pp. 325-346.
• Ohkawa, H., Ohishi, N., Yagi, K. (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95: 351-358. doi: 10.1016/0003-26977990738-3.
• Oja, S.S., Janaky, R., Varga, V., Saranasaari, P. (2000) Modulation of glutamate receptor functions by glutathione. Neurochemistry International 37: 299-306. doi,10.1016/S0197-01860000031-0.
• Özparlak, H. (2013) Effect of seasons on fatty acid composition and ¨ n-3/n-6 ratios of muscle lipids of some fish species in Apa Dam Lake Turkey. Pakistan Journal of Zoology 454: 1027-1033. doi: 0030-9923/2013/0004-1027
• Pereira, J.L., Antunes, S.C., Castro, B.B., Marques, C.R., Goncalves, A.M.M., Goncalves, F., Pereira, R. (2009) Toxicity evaluation of three pesticides on non-target aquatic and soil organisms, commercial formulation versus active ingredient. Ecotoxicology 18(4): 455-463. doi: 10.1007/s10646-009-0300-y
• Persson, J., Vrede, T. (2006) Polyunsaturated fatty acids in zooplankton, variation due to taxonomy and trophic position. Freshwater Biology 51: 887-900. doi: 10.1111/j.1365-2427.2006.01540.x.
• Plourde, M., Cunnane, S.C. (2007) Extremely limited synthe sis of long chain polyunsaturates in adults, Implications for their dietary essentiality and use as supplements. Applied Physiology Nutrition and Metabolism 32: 619-634. doi: 10.1139/H07-034.
• Pryor, W.A. (1989) On the detection of lipid hydroperoxides in biological samples. Free Radical Biology and Medicine 72: 177-178. doi: 10.1016/0891-58498990010-5.Rice, D., Kennedy, S. (1988) Vitamin E function and effects of deficiency. British Veterinary Journal 144: 482-485. doi: 10.1016/0007-19358890089-9.
• Sekino, T., Nakanishi, M., Ishida, Y., Isomura, S., Tsuge, S. Ohtani, H., Kimoto T. (1997) Inter- and intraspecific differences in fatty acid composition of freshwater crustacean zooplankton. Freshwater Biology 38: 611-618. doi: 10.1046/j.1365-2427.1997.00240.x.
• Sellami, I., Guermazi, W., Hamza, A., Aleya, L., Ayadi, H. (2010) Seasonal dynamics of zooplankton community in four Mediterranean reservoirs in humid area Beni Mtir, north of Tunisia and semi arid area Lakhmes Nabhana and Sidi Saâd, center of Tunisia. Journal of Thermal Biology 35(8): 392-400. doi: 10.1016/j.jtherbio.2010.08.004.
• Shalaby, M.A., El Zorba, H.Y., Kamel, G.M. (2004) Effect of α-tocopherol and simvastatin on male fertility in hypercholesterolemic rat. Pharmacological Research 50(2): 137-142. doi,10.1016/j.phrs.2003.10.013.
• Smirnov, N.N. (2014) The physiology of the Cladocera. Amsterdam, Academic Press. 352 p.
• Smyntek, P.M., Teece, M.A., Schulz, K.L., Storch, A.J. (2008) Taxonomic differences in the essential fatty acid composition of groups of freshwater zoop lankton relate to reproductive demands and generation time. Freshwater Biology 53: 1768-1782. doi: 10.1111/j.1365-2427.2008.02001.x.
• Sperfeld E., Wacker A. (2014) Effects of temperature and dietary sterol availability on growth and cholesterol allocation of the aquatic keystone species Daphinia. The Journal of Experimental Biology 212: 3051-3059. doi: 10.1242/jeb.031401.
• Sterner, R.W., Smith, R.F. (1993) Clearance ingestion and release of N and P by Daphnia obtusa feeding on Scenedesmus acutus of varying quality. Bulletin of Marine Science 53: 228-239. Şahan, A., Kurutaş, E., Dikel, S. (2003) Liver Antioxidant Systems and Lipid Peroxidation in Sea Bass Dicentrarchus labrax Adapted to Fresh Water. Turkish Journal of Veterinary and Animal Sciences 27: 1261-1267. Şen Özdemir, N., Caf, F. (2015a) Fatty acid content of Cyclops vicinus in Bingöl Floating Island. Yunus Research Bulletin 3: 3-11 (in Turkish) doi: 10.17693/yunus.06110.
• Şen Özdemir, N., Caf, F. (2015b) Zooplankton Fauna of Bingöl Floating Islands in Winter Season. Journal of Aquaculture Engineering and Fisheries Researches 13: 125-132 ( in Turkish). doi: 10.3153/JAEFR15013.
• Taipale, S.J., Kainz, M.J., Brett, M.T. (2011) Diet-switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in Daphnia. Oikos 120: 1674–1682. doi: 10.1111/j.1600-0706.2011.19415.x
• Tocher, D.R., Leaver, M.J., Hodgson, P.A. (1998) Recent advances in the biochemistry and molecular biology of fatty acyl desaturase. Progress in Lipid Research 37: 73-117. doi: 10.1016/S0163-78279800005-8.
• Viarengo, A., Canesi, L., Pertic,a M., Livingstone, D.R., Orunesi, M. (1999) Age-related lipid peroxidation in the digestive gland of mussels, The role of the antioxidant defence systems. Cellular and Molecular Life Sciences CMLS 475: 454-457. doi: 10.1007/BF01959942
• Vidal, T., Abrantes, N., Gonçalves, A.M.M., Goncalves, F. (2012) Acute and chronic toxicity of Betanal Expert andits active ingredients innontarget aquatic organisms from different trophic levels. Environmental Toxicology 27(9): 537–548.
• Volkman, J.K. (2003) Sterols in microorganisms. Applied Microbiology and Biotechnology 60: 495–506. doi: 10.1007/s00253-002-1172-8
• Von Elert, E. (2002) Determination of limiting polyunsaturated fatty acids in Daphnia galeata using a new method to enrich food algae with single fatty acids. Limnology and Oceanography 47: 1764-1773. doi, 10.4319/lo.2002.47.6.1764.
• Von Elert, E., Martin-Creuzburg, D., Lecoz, J.R. (2003) Absence of Sterols Constrains Carbon Transfer between Cyanobacteria and a Freshwater Herbivore Daphnia galeata. Proceedings of the Royal Society B, Biological Sciences 270: 1209-1214. doi: 10.1098/rspb.2003.2357.
• Wacker, A., Von Elert, E. (2001) Polyunsaturated fatty acids, evidence for nonsubstitutable biochemical resources in Daphnia galeata. Ecology 82: 2507-2520. doi: 10.2307/2679932.
• Wall, R., Ross, R.P., Fitzgerald, G.F., Stanton, C. (2010) Fatty acids from fish, the antiinflammatory potential of longchain omega3 fatty acids. Nutrition Reviews 68: 280-289. doi: 10.1111/j.1753-4887.2010.00287.x.
• Weers, P.M.M., Siewertsen, K., Gulati, R.D. (1997). Is the fatty acid composition of Daphnia galeata determined by the fatty acid composition of the ingested diet? Freshwater Biology 38: 731–738. doi: 10.1046/j.1365-2427.1997.00238.x
• Whitman, R.L., Nevers, M.B., Goodrich, M.L., Murphy, P.C., Davis, B.M. (2004) Characterization of Lake Michigan coastal lakes using zooplankton assemblages. Ecological Indicators 4: 277-286. doi: 10.1016/j.ecolind.2004.08.001.
• Willis, K.J., Ling, N., Chapman, M.A. (1995) Effects of temperature and chemical formulation on the acute toxicity of pentachlorophenol to Simocephalus vetulus Schoedler 1858 Crustacea, Cladocera. New Zealand Journal of Marine and Freshwater Research 29: 289-294. doi: 10.1080/00288330.1995.9516662.
• Zaia, D.A.M., Zaia, C.T.B.V., Lichting, J. (1998) Determination of total protein by spectrophotometry, advantages and disadvantages of proposed methods. Quimica Nova 21(6): 787-793. doi: 10.1590/S0100-40421998000600020